Genetic Evidence That Captured Retroviral Envelope syncytins Contribute to Myoblast Fusion and Muscle Sexual Dimorphism in Mice

PLoS Genetics

Volumn 12, Issue 9, 2016, Pages

  Redelsperger, François ^a,b   Raddi, Najat ^a,b   Bacquin, Agathe ^a,b   Vernochet, Cécile ^a,b   Mariot, Virginie ^c,d,e,f   Gache, Vincent ^g,h,i   Blanchard Gutton, Nicolas ^g,h,i   Charrin, Stéphanie ^b,j   Tiret, Laurent ^g,h,i   Dumonceaux, Julie ^c,d,e,f   Dupressoir, Anne ^a,b   Heidmann, Thierry ^a,b  

^a INSTITUT GUSTAVE ROUSSY   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d Sorbonne Université   (France)

^e CNRS   (France)

^f Institut de Myologie   (France)

^g INSERM U955   (France)

^h UNIVERSITÉ PARIS EST   (France)

ⁱ FACULTÉ DE MÉDECINE   (France)

^j Centre National de la Recherche Scientifique   (France)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOTOXIN; CELL MARKER; SMALL INTERFERING RNA; SYNCYTIN A PROTEIN; SYNCYTIN B PROTEIN; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; PLACENTA PROTEIN; SYNCYTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CELL FUSION; CONTROLLED STUDY; DOG; EX VIVO STUDY; FEMALE; GENE FUNCTION; GENE SILENCING; HUMAN; HUMAN CELL; IN VIVO STUDY; KNOCKOUT MOUSE; MALE; MOUSE; MURINE; MUSCLE DEVELOPMENT; MUSCLE MASS; MUSCLE REGENERATION; MYOBLAST; NONHUMAN; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; QUANTITATIVE TRAIT; REAL TIME POLYMERASE CHAIN REACTION; SEX DIFFERENCE; SHEEP; SYNCYTIN GENE; SYNCYTIUM; UPREGULATION; VIRUS GENE; ANIMAL; CELL DIFFERENTIATION; ENDOGENOUS RETROVIRUS; GENE INACTIVATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MAMMAL; METABOLISM; REGENERATION; SEXUAL DEVELOPMENT; SKELETAL MUSCLE;

ANIMALS; CELL DIFFERENTIATION; DOGS; ENDOGENOUS RETROVIRUSES; FEMALE; GENE KNOCKOUT TECHNIQUES; GENE PRODUCTS, ENV; HUMANS; MALE; MAMMALS; MICE; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; MYOBLASTS; PREGNANCY PROTEINS; REGENERATION; RNA, SMALL INTERFERING; SEX CHARACTERISTICS;

EID: 84990250719     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1006289     Document Type: Article

References (37)

1. Lavialle C, Cornelis G, Dupressoir A, Esnault C, Heidmann O, Vernochet C, et al. Paleovirology of 'syncytins', retroviral env genes exapted for a role in placentation. Philosophical Transactions of the Royal Society B-Biological Sciences. 2013;368(1626). doi: ARTN 20120507 doi: 10.1098/rstb.2012.0507. WOS:000331222100010.
2. Cornelis G, Heidmann O, Bernard-Stoecklin S, Reynaud K, Veron G, Mulot B, et al. Ancestral capture of syncytin-Car1, a fusogenic endogenous retroviral envelope gene involved in placentation and conserved in Carnivora. Proc Natl Acad Sci U S A. 2012;109(7):E432–41. doi: 10.1073/pnas.111534610922308384; PubMed Central PMCID: PMC3289388.
3. Cornelis G, Heidmann O, Degrelle SA, Vernochet C, Lavialle C, Letzelter C, et al. Captured retroviral envelope syncytin gene associated with the unique placental structure of higher ruminants. Proc Natl Acad Sci U S A. 2013;110(9):E828–37. doi: 10.1073/pnas.121578711023401540; PubMed Central PMCID: PMC3587263.
4. Cornelis G, Vernochet C, Carradec Q, Souquere S, Mulot B, Catzeflis F, et al. Retroviral envelope gene captures and syncytin exaptation for placentation in marsupials. Proc Natl Acad Sci U S A. 2015;112(5):E487–96. doi: 10.1073/pnas.141700011225605903; PubMed Central PMCID: PMC4321253.
5. Cornelis G, Vernochet C, Malicorne S, Souquere S, Tzika AC, Goodman SM, et al. Retroviral envelope syncytin capture in an ancestrally diverged mammalian clade for placentation in the primitive Afrotherian tenrecs. Proc Natl Acad Sci U S A. 2014;111(41):E4332–41. doi: 10.1073/pnas.141226811125267646; PubMed Central PMCID: PMC4205661.
6. Dupressoir A, Marceau G, Vernochet C, Benit L, Kanellopoulos C, Sapin V, et al. Syncytin-A and syncytin-B, two fusogenic placenta-specific murine envelope genes of retroviral origin conserved in Muridae. Proc Natl Acad Sci U S A. 2005;102(3):725–30. doi: 10.1073/pnas.040650910215644441; PubMed Central PMCID: PMC545540.
7. Dupressoir A, Vernochet C, Bawa O, Harper F, Pierron G, Opolon P, et al. Syncytin-A knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retrovirus-derived, envelope gene. Proc Natl Acad Sci U S A. 2009;106(29):12127–32. doi: 10.1073/pnas.090292510619564597; PubMed Central PMCID: PMC2715540.
8. Dupressoir A, Vernochet C, Harper F, Guegan J, Dessen P, Pierron G, et al. A pair of co-opted retroviral envelope syncytin genes is required for formation of the two-layered murine placental syncytiotrophoblast. Proc Natl Acad Sci U S A. 2011;108(46):E1164–73. doi: 10.1073/pnas.111230410822032925; PubMed Central PMCID: PMC3219115.
9. Abmayr SM, Pavlath GK, Myoblast fusion: lessons from flies and mice. Development. 2012;139(4):641–56. doi: 10.1242/dev.06835322274696; PubMed Central PMCID: PMC3265056.
10. Bentzinger CF, Wang YX, Rudnicki MA, Building muscle: molecular regulation of myogenesis. Cold Spring Harb Perspect Biol. 2012;4(2). doi: 10.1101/cshperspect.a00834222300977; PubMed Central PMCID: PMC3281568.
11. Buckingham M, Myogenic progenitor cells and skeletal myogenesis in vertebrates. Curr Opin Genet Dev. 2006;16(5):525–32. doi: 10.1016/j.gde.2006.08.00816930987.
12. Buckingham M, Rigby PW, Gene regulatory networks and transcriptional mechanisms that control myogenesis. Dev Cell. 2014;28(3):225–38. doi: 10.1016/j.devcel.2013.12.02024525185.
13. Chen EH, Olson EN, Unveiling the mechanisms of cell-cell fusion. Science. 2005;308(5720):369–73. doi: 10.1126/science.110479915831748.
14. Soe K, Andersen TL, Hobolt-Pedersen AS, Bjerregaard B, Larsson LI, Delaisse JM, Involvement of human endogenous retroviral syncytin-1 in human osteoclast fusion. Bone. 2011;48(4):837–46. doi: 10.1016/j.bone.2010.11.01121111077.
15. Bjerregard B, Ziomkiewicz I, Schulz A, Larsson LI, Syncytin-1 in differentiating human myoblasts: relationship to caveolin-3 and myogenin. Cell Tissue Res. 2014;357(1):355–62. doi: 10.1007/s00441-014-1930-924902667.
16. Yin H, Price F, Rudnicki MA, Satellite cells and the muscle stem cell niche. Physiol Rev. 2013;93(1):23–67. doi: 10.1152/physrev.00043.201123303905; PubMed Central PMCID: PMC4073943.
17. Millay DP, Sutherland LB, Bassel-Duby R, Olson EN, Myomaker is essential for muscle regeneration. Genes Dev. 2014;28(15):1641–6. doi: 10.1101/gad.247205.11425085416; PubMed Central PMCID: PMC4117939.
18. Millay DP, O'Rourke JR, Sutherland LB, Bezprozvannaya S, Shelton JM, Bassel-Duby R, et al. Myomaker is a membrane activator of myoblast fusion and muscle formation. Nature. 2013;499(7458):301–5. doi: 10.1038/nature1234323868259; PubMed Central PMCID: PMC3739301.
19. Keefe AC, Lawson JA, Flygare SD, Fox ZD, Colasanto MP, Mathew SJ, et al. Muscle stem cells contribute to myofibres in sedentary adult mice. Nat Commun. 2015;6:7087. Epub 2015/05/15. ncomms8087 [pii] doi: 10.1038/ncomms808725971691; PubMed Central PMCID: PMC4435732.
20. Darr KC, Schultz E, Hindlimb suspension suppresses muscle growth and satellite cell proliferation. J Appl Physiol (1985). 1989;67(5):1827–34. 2600016.
21. Mozdziak PE, Pulvermacher PM, Schultz E, Unloading of juvenile muscle results in a reduced muscle size 9 wk after reloading. J Appl Physiol (1985). 2000;88(1):158–64. 10642376.
22. Rosenblatt JD, Parry DJ, Adaptation of rat extensor digitorum longus muscle to gamma irradiation and overload. Pflugers Arch. 1993;423(3–4):255–64. 8321629.
23. Lepper C, Conway SJ, Fan CM, Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature. 2009;460(7255):627–U94. doi: 10.1038/nature08209. WOS:000268454300050. 19554048
24. Frese S, Ruebner M, Suhr F, Konou TM, Tappe KA, Toigo M, et al. Long-Term Endurance Exercise in Humans Stimulates Cell Fusion of Myoblasts along with Fusogenic Endogenous Retroviral Genes In Vivo. PLoS One. 2015;10(7):e0132099. Epub 2015/07/15. doi: 10.1371/journal.pone.0132099 PONE-D-15-02026 [pii]. 26154387; PubMed Central PMCID: PMC4495930.
25. Heidmann O, Vernochet C, Dupressoir A, Heidmann T, Identification of an endogenous retroviral envelope gene with fusogenic activity and placenta-specific expression in the rabbit: a new "syncytin" in a third order of mammals. Retrovirology. 2009;6:107. doi: 10.1186/1742-4690-6-10719943933; PubMed Central PMCID: PMC2789053.
26. Georgiadis V, Stewart HJ, Pollard HJ, Tavsanoglu Y, Prasad R, Horwood J, et al. Lack of galectin-1 results in defects in myoblast fusion and muscle regeneration. Dev Dyn. 2007;236(4):1014–24. doi: 10.1002/dvdy.2112317366633.
27. Hamoud N, Tran V, Croteau LP, Kania A, Cote JF, G-protein coupled receptor BAI3 promotes myoblast fusion in vertebrates. Proc Natl Acad Sci U S A. 2014;111(10):3745–50. doi: 10.1073/pnas.131388611124567399; PubMed Central PMCID: PMC3956190.
28. Shilagardi K, Li S, Luo F, Marikar F, Duan R, Jin P, et al. Actin-propelled invasive membrane protrusions promote fusogenic protein engagement during cell-cell fusion. Science. 2013;340(6130):359–63. doi: 10.1126/science.123478123470732; PubMed Central PMCID: PMC3631436.
29. MacLean HE, Chiu WS, Notini AJ, Axell AM, Davey RA, McManus JF, et al. Impaired skeletal muscle development and function in male, but not female, genomic androgen receptor knockout mice. FASEB J. 2008;22(8):2676–89. doi: 10.1096/fj.08-10572618390925.
30. Anson-Cartwright L, Dawson K, Holmyard D, Fisher SJ, Lazzarini RA, Cross JC, The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat Genet. 2000;25(3):311–4. doi: 10.1038/7707610888880.
31. Simmons DG, Natale DR, Begay V, Hughes M, Leutz A, Cross JC, Early patterning of the chorion leads to the trilaminar trophoblast cell structure in the placental labyrinth. Development. 2008;135(12):2083–91. doi: 10.1242/dev.02009918448564; PubMed Central PMCID: PMC3159581.
32. Kadi F, Thornell LE, Concomitant increases in myonuclear and satellite cell content in female trapezius muscle following strength training. Histochemistry and Cell Biology. 2000;113(2):99–103. doi: 10.1007/s004180050012. WOS:000086163600004. 10766262
33. Serra C, Tangherlini F, Rudy S, Lee D, Toraldo G, Sandor NL, et al. Testosterone improves the regeneration of old and young mouse skeletal muscle. J Gerontol A Biol Sci Med Sci. 2013;68(1):17–26. doi: 10.1093/gerona/gls08322499765; PubMed Central PMCID: PMC3598367.
34. Sinha-Hikim I, Cornford M, Gaytan H, Lee ML, Bhasin S, Effects of testosterone supplementation on skeletal muscle fiber hypertrophy and satellite cells in community-dwelling older men. J Clin Endocrinol Metab. 2006;91(8):3024–33. doi: 10.1210/jc.2006-035716705073.
35. Joubert Y, Tobin C, Satellite cell proliferation and increase in the number of myonuclei induced by testosterone in the levator ani muscle of the adult female rat. Dev Biol. 1989;131(2):550–7. 2912808.
36. Sinha-Hikim I, Roth SM, Lee MI, Bhasin S, Testosterone-induced muscle hypertrophy is associated with an increase in satellite cell number in healthy, young men. Am J Physiol Endocrinol Metab. 2003;285(1):E197–205. doi: 10.1152/ajpendo.00370.200212670837.
37. Rando TA, Blau HM, Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy. J Cell Biol. 1994;125(6):1275–87. 8207057; PubMed Central PMCID: PMC2290930.