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Low Molecular weight Proteins in Eukaryotic Genomes that are Encoded by Smorf, with Particular Emphasis on Insect Reproductive Proteins

Kiran Kumar Halagur Bhogegowda, Kiran Kumar D.J, Sajida Niketh, Sowmyashree B.S.

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Indian Journal of Genetics and Molecular Research 13(2):p 69-84, Oct - Dec. 2024. | DOI: https://doi.org/10.21088/ijgmr.2319.4782.13124.2

How Cite This Article:

Bhogegowda KKH, Kumar DJ, Niketh S, et al. Low molecular weight proteins in eukaryotic genomes that are encoded by smORF, with particular emphasis on insect reproductive proteins. Ind J Genet Mol Res. 2024;13(1):69-84.

Timeline

Received : October 22, 2024         Accepted : November 25, 2024          Published : December 30, 2024

Abstract

The majority of non-repetitive DNA in higher eukaryote genomes is transcribed, but only a small portion of them code for proteins, which appears to be a conundrum. The term "smORF-encoded proteins" (SEPs) refers to small open reading frames (smORFs) that encode functional proteins and are located across the genome in various locations, such as coding sequences (CDSs) and the 5' and 3' untranslated regions (UTRs) of genes. Numerous vital processes, such as metabolic, cellular, gene expression, embryogenesis and development are carried out by SEPs. Additionally, they are connected to a number of clinical conditions promote proteome evolution. As omics technology and identification techniques progress, a large number of peptides are currently being annotated. Further, several of these peptides are essential for the regulation of reproductive physiology and development in insects. Male seminal fluid proteins (SFPs) elicit a physiological response in the females during mating that increases the reproductive success of the mating pair. This response is known as the post-mating response (PMR). SFPs exhibit a broad distribution of relative molecular weights and influence a variety of functions, including catalysis, inhibitor activity, and protein folding and binding. It is now known that several of these proteins, such as MSAmiP in Drosophila, are crucial to insect reproduction. The area of smorf is reviewed in this mini-review, covering basic biology, mechanisms and functions, methodology and advancements finally evolutionary trends. Further expansion of the discussion to their involvement in insect reproductive physiology is also included.


References

  • 1.   C. P. Ponting, P. L. Oliver, W. Reik, Evolution and functions of long noncoding RNAs.
  • 2.   Cell.2009. 136. 629–641.
  • 3.   Clement Immarigeon,Yohan Frei, Sofie Y. N. and Robert K. Maeda.Identification of a micropeptide and multiple secondary cell genes that modulate Drosophila male reproductive success. Proc Natl Acad Sci U S A. 2021 Apr 13;118(15):e2001897118. doi: 10.1073/pnas.2001897118 https://doi. org/10.1073/pnas.2001897118;.
  • 4.   Emmanuel Ladoukakis, Vini Pereira, Emile G Magny, Adam Eyre-Walker & Juan Pablo Couso. Hundreds of putatively functional small open reading frames in Drosophila. Genome Biol. 2011. 12, R118.
  • 5.   Alvaro de Andres-Pablo, Antonin Morillon, Maxime Wery. LncRNAs, lost in translation or licence to regulate?.Curr. Genet. 2017.63.29–3.
  • 6.   Diego Guerra-Almeida, Diogo Antonio Tschoeke, Rodrigo Nunes-da-Fonseca.Understanding small ORF diversity through a comprehensive transcription feature classification.DNA Res. 2021 Jul 7;28(5):dsab007. doi: 10.1093/dnares/dsab007.
  • 7.   Ruth Steinberg, Hans-Georg Koch. The largely unexplored biology of small proteins in pro- and eukaryotes.FEBS J. 2021 Dec;288(24):7002-7024. doi: 10.1111/febs.15845. Epub 2021 Jun 8.
  • 8.   Catherine A Makarewich. The hidden world of membrane microproteins.Exp Cell Res. 2020 Mar 15;388(2):111853. doi: 10.1016/j.yexcr.2020.111853. Epub 2020 Jan 21.
  • 9.   Nausica Arnoult, Adriana Correia, Jiao Ma, Anna Merlo, Sara Garcia-Gomez, Marija Maric, Marco Tognetti, Christopher W Benner, Simon J Boulton, Alan Saghatelian, Jan Karlseder.Regulation of DNA repair pathway choice in S and G2 phases by the NHEJ inhibitor CYREN.Nature. 2017 Sep 20;549(7673):548-552. doi: 10.1038/nature24023.
  • 10.   Y Wang, R Benezra, DA Sassoon. Id expression during mouse development: a role in morphogenesis.Dev Dyn. 1992 Jul;194(3):222-30. doi: 10.1002/aja.1001940307.
  • 11.   Kaushal Kumar Bhati, Anko Blaakmeer, Esther Botterweg Paredes, Ulla Dolde, Tenai Eguen, ShinYoung Hong, Vandasue Rodrigues, Daniel Straub, Bin Sun, Stephan Wenkel.Approaches to identify and characterize microProteins and their potential uses in biotechnology. Cell Mol Life Sci. 2018 Jul;75(14):2529-2536. doi: 10.1007/s00018-018-2818- 8. Epub 2018 Apr 18.
  • 12.   Munira A Basrai, Victor E Velculescu, Kenneth W Kinzler, Philip Hieter.NORF5/HUG1 is a component of the MEC1-mediated checkpoint response to DNA damage and replication arrest in Saccharomyces cerevisiae. Mol Cell Biol. 1999 Oct;19(10):7041-9. doi: 10.1128/MCB.19.10.7041.
  • 13.   Jiang Zhu, Shiyi Wang, Cheng Wang, Zhi Wang, Gan Luo, Junhui Li, Yangyang Zhan, Dongbo Cai, Shouwen Chen.Microbial synthesis of bacitracin: Recent progress, challenges, and prospects.Synth Syst Biotechnol. 2023 Apr 10;8(2):314-322. doi: 10.1016/j.synbio.2023.03.009. eCollection 2023 Jun.
  • 14.   Annie Rathore, Qian Chu, Dan Tan, Thomas F Martinez, Cynthia J Donaldson, Jolene K Diedrich, John R Yates, Alan Saghatelian.MIEF1 Microprotein Regulates Mitochondrial Translation Biochemistry. 2018 Sep 25;57(38):5564-5575. doi: 10.1021/acs. biochem.8b00726. Epub 2018 Sep 14.
  • 15.   Yoo-Seok Hwang, Hyun-Shik Lee, Teddy Kamata, Kathleen Mood, Hee Jun Cho, Emily Winterbottom, Yon Ju Ji, Arvinder Singh, Ira O Daar.The Smurf ubiquitin ligases regulate tissue separation via antagonistic interactions with ephrinB1.Genes Dev. 2013 Mar 1;27(5):491-503. doi: 10.1101/ gad.208355.112.
  • 16.   Jose I Pueyo, Emile G Magny, Christopher J Sampson, Unum Amin, Iwan R Evans, Sarah A Bishop, Juan P Couso.Hemotin, a Regulator of Phagocytosis Encoded by a Small ORF and Conserved across Metazoans.PLoS Biol. 2016 Mar 25;14(3):e1002395. doi: 10.1371/journal.pbio.1002395. eCollection 2016 Mar.
  • 17.   Sarah A Slavoff, Jinho Heo, Bogdan A Budnik, Leslyn A Hanakahi, Alan Saghatelian. Human Short Open Reading Frame (sORF)-encoded Polypeptide That Stimulates DNA End Joining.J Biol Chem. 2014 Apr 18; 289(16): 10950–10957.Published online 2014 Mar 7. doi: 10.1074/jbc.C113.533968.
  • 18.   Nadia G D’Lima, Jiao Ma, Lauren Winkler, Qian Chu, Ken H Loh, Elizabeth O Corpuz, Bogdan A Budnik, Jens Lykke-Andersen, Alan Saghatelian, Sarah A Slavoff.A human microprotein that interacts with the mRNA decapping complexNat Chem Biol. 2017 Feb;13(2):174-180. doi: 10.1038/ nchembio.2249. Epub 2016 Dec 5.
  • 19.   Jose Ignacio Pueyo, Juan Pablo Couso.The 11-aminoacid long Tarsal-less peptides trigger a cell signal in Drosophila leg development.Dev Biol. 2008 Dec 15;324(2):192-201. doi: 10.1016/j. ydbio.2008.08.025. Epub 2008 Sep 5.
  • 20.   Andrea Pauli, Eivind Valen, Alexander F Schier.. Identifying (non-)coding RNAs and small peptides: challenges and opportunities. Bioessays. 2015 Jan;37(1):103-12. doi: 10.1002/bies.201400103. Epub 2014 Oct 24.
  • 21.   Sonam Dhamija & Manoj B. Menon.Non-coding transcript variants of protein-coding genes – what are they good for?, RNA Biology.2018.15:8.1025-1031, DOI:10.1080/15476286.2018.1511675.
  • 22.   Diego Guerra-Almeida, Diogo Antonio Tschoeke, Rodrigo Nunes-da-Fonseca Understanding small ORF diversity through a comprehensive transcription feature classification. DNA Research. 2021. 28(5), 1-18. https://doi.org/10.1093/dnares/ dsab007.
  • 23.   Couso, J. and Patraquim, P. Classification and function of small open reading frames, Nat. Rev. Mol. Cell Biol. 2017. 18. 575–89.
  • 24.   Ladoukakis, E., Pereira, V., Magny, E.G., EyreWalker, A. and Couso, J., Hundreds of putatively functional small open reading frames in Drosophila, Genome Biol. 2011.12. R118. 43.
  • 25.   Hucker, S.M., Ardern, Z., Goldberg, T., et al., Discovery of nu merous novel small genes in the intergenic regions of the Escherichia coli O157:H7 Sakai genome, PLoS One. 2017.12 e0184119.
  • 26.   Friedman, R.C., Kalkhof, S., Doppelt-Azeroual, O., et al., Common and phylogenetically widespread coding for peptides by bacte rial small RNAs, BMC Genomics. 2017.18. 553.
  • 27.   Bronesky, D., Wu, Z., Marzi, S., et al. Staphylococcus aureus RNAIII and its regulon link quorum sensing, stress responses, metabolic adaptation, and regulation of of Virulence Gene Expression.2016. Annu Rev Microbiol. 2016 Sep 8:70:299-316.
  • 28.   Yuji Kageyama, Takefumi Kondo, Yoshiko Hashimoto.Coding vs non-coding: translatability of short ORFs found in putative non-coding transcripts, Biochimie.2011.93, 1981–6.
  • 29.   Kageyama, Y., Kondo, T. and Hashimoto, Y., Coding vs non-coding: translatability of short ORFs found in putative non-coding transcripts, Biochimie. 2011.93.1981–6.
  • 30.   Lauressergues, D., Couzigou, J.-M., Clemente, H.S., et al. Primary transcripts of microRNAs encode regulatory peptides, Nature.2015.520. 90–3.
  • 31.   Pamudurti, N.R., Bartok, O., Jens, M., et al. Translation of CircRNAs, Mol. Cell. 2017.66. 9–21.e7.
  • 32.   Pauli, A., Valen, E. and Schier, A.F. Identifying (non-)coding RNAs and small peptides: challenges and opportunities, Bioessays. 2015. 37 103–12.
  • 33.   Chu, Q., Ma, J. and Saghatelian, A. Identification and characteri zation of sORF-encoded polypeptides, Crit. Rev. Biochem. 2015. Mol. Biol. 50.134–41.
  • 34.   Sasaki, K., Nakamura, Y., Maki, K., et al. Functional analysis of a dominant-negative DETS TEL/ ETV6 isoform, Biochem. Biophys. Res. Commun. 2004.317.1128–37.
  • 35.   Ohno, S. Birth of a unique enzyme from an alternative reading frame of the preexisted, internally repetitious coding sequence, Proc. Natl. Acad. Sci. U S A.1984. 81.2421–5.
  • 36.   Klemke, M., H., Kehlenbach, R. and Huttner, W.B. Two overlap ping reading frames in a single exon encode interacting proteins–a novel way of gene usage, Embo J. 2001. 20. 3849–60.
  • 37.   Vanderperre, B., Lucier, J.-F., Bissonnette, C., et al. Direct detection of alternative open reading frames translation products in human significantly expands the proteome, PLoS One. 2013.8. e70698.
  • 38.   Kochetov, A.V. Alternative translation start sites and hidden coding potential of eukaryotic mRNAs, Bioessays.2008.30,.683–91.
  • 39.   Uenaka, A., Ono, T., Akisawa, T., Wada, H., Yasuda, T. and Nakayama, E. Identification of a unique antigen peptide pRL1 on BALB/c RL male 1 leukemia recognized by cytotoxic T lymphocytes and its relation to the Akt oncogene, J. Exp. Med. 1994.180.1599–607.
  • 40.   Michel, A.M., Choudhury, K.R., Firth, A.E., Ingolia, N.T., Atkins, J.F. and Baranov, P.V. Observation of dually decoded regions of the human genome using ribosome profiling data. Genome Res. 2012 Nov;22(11):2219-29. doi: 10.1101/gr.133249.111. Epub 2012 May 16.
  • 41.   Wang, R.F., Parkhurst, M.R., Kawakami, Y., Robbins, P.F. and Rosenberg, S.A. Utilization of an alternative open reading frame of a normal gene in generating a novel human cancer antigen, J. Exp. Med. 1996. 183. 1131–40.
  • 42.   Mehta, A., Trotta, C.R. and Peltz, S.W. Derepression of the Her-2 uORF is mediated by a novel posttranscriptional control mechanism in cancer cells, Genes Dev. 2006. 20.939–53.
  • 43.   Malarkannan, S., Shih, P.P., Eden, P.A., et al. The molecular and functional characterization of a dominant minor H antigen, H60, J. Immunol. 1998.161. 3501–9.
  • 44.   K. Bharathan Sruthi,Athira Menon, Akash Pakash, Peppurath Vasudevan Soniya.Pervasive translation of small open reading frames in plant long noncoding RNAs.Front Plant Sci. 2022 Oct 24;13:975938. doi: 10.3389/fpls.2022.975938. eCollection 2022.
  • 45.   Marta A Inchingolo, Aurelie Diman, Maxime Adamczewski, Tom Humphreys, Pascale JaquierGuble, Joseph A Curran.TP53BP1, a dual-coding gene, uses promoter switching and translational reinitiation to express a smORF protein.iScience. 2023 Apr 27;26(5):106757. doi: 10.1016/j. isci.2023.106757. eCollection 2023 May 19.
  • 46.   Pedro Patraquim, Emile G. Magny, Jose I. Pueyo, Ana Isabel Platero & Juan Pablo Couso.Translation and natural selection of micropeptides from long non-canonical RNAs.Nature Communications.2022. volume 13, 6515.
  • 47.   Dominique Lauressergues, Jean-Malo Couzigou, Helene San Clemente, Yves Martinez, Christophe Dunand, Guillaume Bécard, Jean-Philippe Combier. Primary transcripts of microRNAs encode regulatory peptidesNature. 2015 Apr 2;520(7545):90- 3. doi: 10.1038/nature14346. Epub 2015 Mar 25.
  • 48.   Julie L Aspden, Ying Chen Eyre-Walker, Rose J Phillips, Unum Amin, Muhammad Ali S Mumtaz, Michele Brocard, Juan-Pablo Couso.Extensive translation of small Open Reading Frames revealed by Poly-Ribo-Seq.Elife. 2014 Aug 21:3:e03528. doi: 10.7554/eLife.03528.
  • 49.   Bersabe Wondimagegnhu,Wen Ma, Tapas Paul, Ting-Wei Liao, Chun Ying Lee, Samantha Sanford, Patricia L Opresko, Sua Myong.The molecular mechanism for TERRA recruitment and annealing to telomeres.Nucleic Acids Res. 2024 Sep 23;52(17):10490-10503. doi: 10.1093/nar/gkae732.
  • 50.   Jingwen Song, Syed Nabeel-Shah, Shuye Pu, Hyunmin Lee, Ulrich Braunschweig, Zuyao Ni, Nujhat Ahmed, Edyta Marcon, Guoqing Zhong,Debashish Ray, Kevin C H Ha, Xinghua Guo, Zhaolei Zhang, Timothy R Hughes, Benjamin J Blencowe,Jack F Greenblatt.Regulation of alternative polyadenylation by the C2H2-zincfinger protein Sp1.Mol Cell. 2022 Sep 1;82(17):3135- 3150.e9. doi: 10.1016/j.molcel.2022.06.031. Epub 2022 Jul 31.
  • 51.   Keira R Hassel, Omar Brito-Estrada, Catherine A Makarewich. Microproteins: Overlooked regulators of physiology and disease.iScience. 2023 Apr 29;26(6):106781. doi: 10.1016/j.isci.2023.106781. eCollection 2023 Jun 16.
  • 52.   Luis Enrique Cabrera-Quio, Sarah Herberg, Andrea Pauli.Decoding sORF translation - from small proteins to gene regulation. RNA Biol. 2016 Nov;13(11):1051-1059. doi: 10.1080/15476286.2016.1218589. Epub 2016 Aug 12.
  • 53.   Rui Vitorino, Sofia Guedes, Francisco Amado, Manuel Santos, Nobuyoshi Akimitsu.. The role of micropeptides in biology.Cell Mol Life Sci. 2021 Apr;78(7):3285-3298. doi: 10.1007/s00018-020- 03740-3. Epub 2021 Jan 28.
  • 54.   Emile G Magny, Jose Ignacio Pueyo, Frances M G Pearl, Miguel Angel Cespedes, Jeremy E Niven, Sarah A Bishop, Juan Pablo CousoConserved regulation of cardiac calcium uptake by peptides encoded in small open reading frames.Science. 2013 Sep 6;341(6150):1116-20. doi: 10.1126/ science.1238802. Epub 2013 Aug 22.
  • 55.   Akinobu Matsumoto, Alessandra Pasut, Masaki Matsumoto, Riu Yamashita, Jacqueline Fung, Emanuele Monteleone, Alan Saghatelian, Keiichi I. Nakayama, John G. Clohessy & Pier Paolo Pandolfi. mTORC1 and muscle regeneration are regulated by the LINC00961-encoded SPAR polypeptide. Nature. 2017 Jan 12;541(7636):228-232. doi: 10.1038/ nature21034. Epub 2016 Dec 26.
  • 56.   Sheng Xu, LuYu Zhou, Murugavel Ponnusamy, LiXia Zhang, YanHan Dong, YanHui Zhang, Qi Wang, Jing Liu, Kun Wang.A comprehensive review of circRNA: from purification and identification to disease marker potential.PeerJ. 2018 Aug 24:6:e5503. doi: 10.7717/peerj.5503. eCollection 2018.
  • 57.   Yanan Pang, Chuanbin Mao,Shanrong Liu. Encoding activities of non-coding RNAs.Theranostics. 2018 Mar 28;8(9):2496-2507. doi: 10.7150/thno.24677. eCollection 2018.
  • 58.   Carina Azevedo Oliveira Silva, Sandy da Silveira Alves, Bruno da Costa Rodrigues, Jonatha Anderson Fraga Egidio, Lupis Ribeiro, Carlos Logullo, Flavia Borges Mury, Daniele das Graças Santos, Taynan Portal, Cintia Monteiro-de-Barros, José Roberto da Silva, José Luciano NepomucenoSilva, Rodrigo Nunes-da-Fonseca.The mlpt smORF gene is essential for digestive physiology and molting during nymphal stages in the kissing bug Rhodnius prolixus.Insect Biochem Mol Biol. 2024 Sep:172:104154. doi: 10.1016/j.ibmb.2024.104154. Epub 2024 Jul 5.
  • 59.   Inaki Merino-Valverde, Emanuela Greco, Maria Abad.The microproteome of cancer: From invisibility to relevance.Exp Cell Res. 2020 Jul 1;392(1):111997. doi: 10.1016/j.yexcr.2020.111997. Epub 2020 Apr 14.
  • 60.   Jia-Rui You, Zeng-Jin Wen, Jia-Wei Tian, XiaoBing Lv, Rong Li, Shu-Ping Li, Hui Xin, Pei-Feng Li, Yin-Feng Zhang, Rui Zhang Crosstalk between ubiquitin ligases and ncRNAs drives cardiovascular disease progression. Front Immunol. 2024; 15: 1335519. Published online 2024 Mar 7. doi: 10.3389/ fimmu.2024.1335519.
  • 61.   Nils G Walter. Are non-protein coding RNAs junk or treasure?: An attempt to explain and reconcile opposing viewpoints of whether the human genome is mostly transcribed into nonfunctional or functional RNAsBioessays. 2024 Apr;46(4):e2300201. doi: 10.1002/bies.202300201. Epub 2024 Feb 13.
  • 62.   https://www.encodeproject.org/help/projectoverview/.
  • 63.   Matthew Putnins, Ioannis P Androulakis. Selfselection of evolutionary strategies: adaptive versus non-adaptive forces. Heliyon. 2021 May 15;7(5):e06997. doi: 10.1016/j.heliyon.2021.e06997. eCollection 2021 May.
  • 64.   W Ford Doolittle, Tyler D P Brunet. On causal roles and selected effects: our genome is mostly junk.BMC Biol. 2017 Dec 5;15(1):116. doi: 10.1186/s12915-017- 0460-9.
  • 65.   Anastasia Chugunova, Elizaveta Loseva, Pavel Mazin, Aleksandra Mitina, Tsimafei Navalayeu, Dmitry Bilan, Polina Vishnyakova, Maria Marey, Anna Golovina, Marina Serebryakova, Philipp Pletnev, Maria Rubtsova, Waltraud Mair, Anna Vanyushkina, Philipp Khaitovich, Vsevolod Belousov, Mikhail Vysokikh, Petr Sergiev, Olga Dontsova.LINC00116 codes for a mitochondrial peptide linking respiration and lipid metabolism. Proc Natl Acad Sci U S A. 2019 Mar 12;116(11):4940- 4945. doi: 10.1073/pnas.1809105116. Epub 2019 Feb 22.
  • 66.   Alberto Vassallo, Emilia Palazzotto, Giovanni Renzone, Luigi Botta, Teresa Faddetta, Andrea Scaloni, Anna Maria Puglia, Giuseppe Gallo.The Streptomyces coelicolor Small ORF trpM Stimulates Growth and Morphological Development and Exerts Opposite Effects on Actinorhodin and Calcium-Dependent Antibiotic Production. Front Microbiol. 2020 Feb 19:11:224. doi: 10.3389/ fmicb.2020.00224. eCollection 2020.
  • 67.   Benoit Vanderperre, Jean-Francois Lucier, Cyntia Bissonnette, Julie Motard, Guillaume Tremblay, Solene Vanderperre, Maxence Wisztorski, Michel Salzet, François-Michel Boisvert, Xavier RoucouDirect detection of alternative open reading frames translation products in human significantly expands the proteome.PLoS One. 2013 Aug 12;8(8):e70698. doi: 10.1371/journal.pone.0070698. eCollection 2013.
  • 68.   Zhe Ji, Ruisheng Song, Aviv Regev, Kevin Struhl. Many lncRNAs, 5’UTRs, and pseudogenes are translated and some are likely to express functional proteins. eLife.2015. 4:e08890. doi: 10.7554/ eLife.08890.
  • 69.   Aaron Wacholder, Saurin Bipin Parikh, Nelson Castilho Coelho, Omer Acar, Carly Houghton, Lin Chou, Anne-Ruxandra Carvunis..A vast evolutionarily transient translatome contributes to phenotype and fitness.Cell Syst. 2023 May 17;14(5):363-381.e8. doi: 10.1016/j.cels.2023.04.002. Epub 2023 May 9.
  • 70.   Mudge JM, Ruiz-Orera J, Prensner JR, Brunet MA, Gonzalez JM, Magrane M, et al. A community-driven roadmap to advance research on translated open reading frames detected by Ribo-seq. bioRxiv. 2021;2021.06.10.447896. http://biorxiv.org/ content/early/2021/06/10/ 2021.06.10.447896. abstract.
  • 71.   McLysaght A, Hurst LD. Open questions in the study of de novo genes: what, how and why. Nat Rev Genet. 2016;17:567–78. https://doi.org/10. 1038/nrg.2016.78.
  • 72.   Ingolia NT, Ghaemmaghami S, Newman JRS, Weissman JS. Genomewide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science. 2009;324:218.
  • 73.   Aspden JL, Eyre-Walker YC, Phillips RJ, Amin U, Mumtaz MAS, Brocard M, et al. Extensive translation of small open reading frames revealed by poly-ribo-seq. Elife. 2014;3:1–19.
  • 74.   Lopez E, Wang X, Madero L, Lopez-Pascual J, Latterich M. Functional phosphoproteomic mass spectrometry-based approaches. Clin Transl Med. 2012. https://doi.org/10.1186/2001- 1326-1- 20.
  • 75.   Low TY, Heck AJ. Reconciling proteomics with next generation sequencing. Curr Opin Chem Biol. 2016;30:14–20.
  • 76.   Cao X, Khitun A, Na Z, Dumitrescu DG, Kubica M, Olatunji E, et al. Comparative proteomic profiling of unannotated microproteins and alternative proteins in human cell lines. J Proteome Res Am Chem Soc.
  • 77.   2020;19:3418–26.
  • 78.   Lee C, Kim KH, Cohen P. MOTS-c: a novel mitochondrial-derived peptide regulating muscle and fat metabolism. Free Radic Biol Med. 2016. https://doi.org/10.1016/j. freeradbiomed.2016.05.015.
  • 79.   ChenJ, Brunner A-D, Cogan JZ, Nunez JK, Fields AP, Adamson B, et al. Pervasive functional translation of non-canonical human open reading frames. Science (80-). 2020;367:1140–6.
  • 80.   Stein CS, Jadiya P, Zhang X, McLendon JM, Abouassaly GM, Witmer NH, et al. Mitoregulin: a lncRNA-encoded microprotein that supports mitochondrial supercomplexes and respiratory efficiency. Cell Rep. 2018;23:3710–37208.
  • 81.   Fabiola Valdivia-Francia, Ataman Sendoel.No country for old methods: New tools for studying microproteins.iScience. 2024 Jan 20;27(2):108972. doi: 10.1016/j.isci.2024.108972. eCollection 2024 Feb 16.
  • 82.   L A Herndon, M F Wolfner. A Drosophila seminal fluid protein, Acp26Aa, stimulates egg laying in females for 1 day after mating.Proc Natl Acad Sci U S A. 1995 Oct 24;92(22):10114-8. doi: 10.1073/ pnas.92.22.10114.
  • 83.   Frank W Avila, Laura K Sirot, Brooke A LaFlamme, C Dustin Rubinstein, Mariana F Wolfner. Insect seminal fluid proteins: identification and function. Annu Rev Entomol. 2011; 56: 21-40. doi: 10.1146/ annurev-ento-120709-144823.
  • 84.   K Ravi Ram, Mariana F Wolfner. Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction. Integr Comp Biol. 2007 Sep;47(3):427-45. doi: 10.1093/icb/icm046. Epub 2007 Jun 1.
  • 85.   Tracey Chapman. Sexual Conflict: Mechanisms and Emerging Themes in Resistance Biology.Am Nat. 2018 Aug;192(2):217-229. doi: 10.1086/698169. Epub 2018 May 24.
  • 86.   Steven A Ramm, Lucy McDonald, Jane L Hurst, Robert J Beynon, Paula StockleyComparative proteomics reveals evidence for evolutionary diversification of rodent seminal fluid and its functional significance in sperm competition. Mol Biol Evol. 2009 Jan;26(1):189-98. doi: 10.1093/ molbev/msn237. Epub 2008 Oct 17.
  • 87.   Laura K Sirot, Alex Wong, Tracey Chapman, Mariana F Wolfner.Sexual conflict and seminal fluid proteins: a dynamic landscape of sexual interactions.Cold Spring Harb Perspect Biol. 2014 Dec 11;7(2):a017533. doi: 10.1101/cshperspect. a017533.
  • 88.   Jolie A Carlisle, Willie J Swanson.Molecular mechanisms and evolution of fertilization proteins.J Exp Zool B Mol Dev Evol. 2021 Dec;336(8):652-665. doi: 10.1002/jez.b.23004. Epub 2020 Oct 4.
  • 89.   Mrinalini, Cho Yeow Koh, Nalini Puniamoorthy. Rapid Genomic Evolution Drives the Diversification of Male Reproductive Genes in Dung Beetles. Genome Biol Evol. 2021 Aug; 13(8): evab172. Published online 2021 Jul 28. doi: 10.1093/gbe/ evab172.
  • 90.   Seirian Sumner, Emeline Favreau, Katherine Geist, Amy L. Toth, Sandra M. Rehan.Molecular patterns and processes in evolving sociality: lessons from insects. Philos Trans R Soc Lond B Biol Sci. 2023; April 10, 378(1874): 20220076. Published online February 20, 2023. doi: 10.1098/rstb.2022.0076.
  • 91.   Patlar B, Civetta A.Seminal fluid gene expression and reproductive fitness in Drosophila melanogaster. BMC Ecol Evol. 2022 Feb 23;22(1):20. doi: 10.1186/ s12862-022-01975-1.
  • 92.   Martin D Garlovsky, Yasir H Ahmed-Braimah. Evolutionary Quantitative Proteomics of Reproductive Protein Divergence in Drosophila. Mol Cell Proteomics. 2023 Aug;22(8):100610. doi: 10.1016/j.mcpro.2023.100610. Epub 2023 Jun 28.
  • 93.   Papachristos K, Sayadi A, Arnqvist G.Comparative Genomic Analysis of the Pattern of Evolution of Male and Female Reproductive Proteins in Seed Beetles. Genome Biol Evol. 2024 Jul 3;16(7):evae143. doi: 10.1093/gbe/evae143.
  • 94.   Brittany L. Enzmann, Peter Nonacs. Optimists or realists? How ants allocate resources in making reproductive investments.J Anim Ecol. 2018 Jul;87(4):1126-1136. doi: 10.1111/1365-2656.12840. Epub 2018 May 29.
  • 95.   Ruiz-Orera J, Albà MM.Translation of Small Open Reading Frames: Roles in Regulation and Evolutionary Innovation.Trends Genet. 2019 Mar;35(3):186-198. doi: 10.1016/j.tig.2018.12.003. Epub 2018 Dec 31.
  • 96.   Juan-Pablo Couso, Pedro Patraquim.Classification and function of small open reading frames.Nat Rev Mol Cell Biol. 2017 Sep;18(9):575-589. doi: 10.1038/ nrm.2017.58. Epub 2017 Jul 12.
  • 97.   Emmanuel Ladoukakis, Vini Pereira, Emile G Magny, Adam Eyre-Walker & Juan Pablo Couso. Hundreds of putatively functional small open reading frames in Drosophila.Genome Biol. 2011 Nov 25;12(11):R118. doi: 10.1186/gb-2011-12- 11-r118.
  • 98.   Azza Dib, Jennifer Zanet, Alexandra ManchenoFerris, Maylis Gallois, Damien Markus, Philippe Valenti, Simon Marques-Prieto, Serge Plaza, Yuji Kageyama, Hélène Chanut-Delalande, François Payre.Pri smORF Peptides Are Wide Mediators of Ecdysone Signaling, Contributing to Shape Spatiotemporal Responses.Front Genet. 2021 Aug 30:12:714152. doi: 10.3389/fgene.2021.714152. eCollection 2021.
  • 99.   Linrong Wan, Wenfu Xiao, Ziyan Huang, Anlian Zhou, Yaming Jiang, Bangxing Zou, Binbin Liu, Cao Deng, Youhong Zhang..Systematic identification of smORFs in domestic silkworm (Bombyx mori).Peer J. 2023 Jan 13;11:e14682. doi: 10.7717/peerj.14682. eCollection 2023.
  • 100.   Cornelia Fritsch, F Javier Bernardo-Garcia, TimHenning Humberg, Abhishek Kumar Mishra, Sara Miellet, Silvia Almeida, Michael V Frochaux, Bart Deplancke, Armin Huber, Simon G Sprecher. Multilevel regulation of the glass locus during Drosophila eye development.PLoS Genet. 2019 Jul 12;15(7):e1008269. doi: 10.1371/journal. pgen.1008269. eCollection 2019 Jul.
  • 101.   Emile G Magny, Jose Ignacio Pueyo, Frances M G Pearl, Miguel Angel Cespedes, Jeremy E Niven, Sarah A Bishop, Juan Pablo Couso. Conserved regulation of cardiac calcium uptake by peptides encoded in small open reading frames.Science. 2013 Sep 6;341(6150):1116-20. doi: 10.1126/ science.1238802. Epub 2013 Aug 22.
  • 102.   Peter F Renz, Fabiola Valdivia-Francia, Ataman Sendoel..Some like it translated: small ORFs in the 5’UTR.Exp Cell Res. 2020 Nov 1;396(1):112229. doi: 10.1016/j.yexcr.2020.112229. Epub 2020 Aug 17.
  • 103.   Chrysoula-Evangelia Karachaliou and Evangelia Livaniou.Neuroprotective Action of Humanin and Humanin Analogues: Research Findings and Perspectives. Biology (Basel). 2023 Dec; 12(12): 1534.
  • 104.   Hanna Persha, Stephen A Thacker, Krutika Mediwala Hornback, Gustavo R Alvira-Arill, Richard Lueking, Taylor Morrisette. Real-World Clinical Characteristics and Outcomes with Daptomycin Use in Pediatric Patients: A Retrospective Case Series Antibiotics (Basel). 2024 Sep 2;13(9):833. doi: 10.3390/ antibiotics13090833.
  • 105.   Assim A. Alfadda, Anas M. Abdel Rahman,Hicham Benabdel kamel,Reem AlMalki,Bashayr Alsuwayni,Abdulaziz Alhossan,Madhawi M. Aldhwayan,Ghalia N. Abdeen,Alexander Dimitri Miras and Afshan Masood. Metabolomic Effects of Liraglutide Therapy on the Plasma Metabolomic Profile of Patients with Obesity.Metabolites. 2024 Sep 17;14(9):500. doi: 10.3390/metabo14090500.

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There are no additional data available. All raw data and code are available upon request.

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All authors contributed significantly to the work and approve its publication.

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Bhogegowda KKH, Kumar DJ, Niketh S, et al. Low molecular weight proteins in eukaryotic genomes that are encoded by smORF, with particular emphasis on insect reproductive proteins. Ind J Genet Mol Res. 2024;13(1):69-84.


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Received Accepted Published
October 22, 2024 November 25, 2024 December 30, 2024

DOI: https://doi.org/10.21088/ijgmr.2319.4782.13124.2

Keywords

Small open reading frames (smORFs)post-mating response (PMR)evolutionary-constrained domain residues/ regions (ECRs)

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Received October 22, 2024
Accepted November 25, 2024
Published December 30, 2024

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Attribution-Non-commercial 4.0 International (CC BY-NC 4.0)

This license enables reusers to distribute, remix, adapt, and build upon the material in any medium or format for noncommercial purposes only, and only so long as attribution is given to the creator.


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