LINE-1 Mediated Insertion into (Protein of Centriole 1 A) Causes Growth Insufficiency and Male Infertility in Mice

1. Krakow D, Rimoin DL (2010) The skeletal dysplasias. Genet Med 12: 327–341. doi: 10.1097/GIM.0b013e3181daae9b 20556869

2. Karsenty G, Kronenberg HM, Settembre C (2009) Genetic control of bone formation. Annu Rev Cell Dev Biol 25: 629–648. doi: 10.1146/annurev.cellbio.042308.113308 19575648

3. Song B, Haycraft CJ, Seo HS, Yoder BK, Serra R (2007) Development of the post-natal growth plate requires intraflagellar transport proteins. Dev Biol 305: 202–216. 17359961

4. Zhang J, Tan X, Li W, Wang Y, Wang J, et al. (2005) Smad4 is required for the normal organization of the cartilage growth plate. Dev Biol 284: 311–322. 16023633

5. Thiel C, Kessler K, Giessl A, Dimmler A, Shalev SA, et al. (2011) NEK1 mutations cause short-rib polydactyly syndrome type majewski. Am J Hum Genet 88: 106–114. doi: 10.1016/j.ajhg.2010.12.004 21211617

6. Li Y, Dudley AT (2009) Noncanonical frizzled signaling regulates cell polarity of growth plate chondrocytes. Development 136: 1083–1092. doi: 10.1242/dev.023820 19224985

7. Klingseisen A, Jackson AP (2011) Mechanisms and pathways of growth failure in primordial dwarfism. Genes Dev 25: 2011–2024. doi: 10.1101/gad.169037 21979914

8. Warman ML, Cormier-Daire V, Hall C, Krakow D, Lachman R, et al. (2011) Nosology and classification of genetic skeletal disorders: 2010 revision. Am J Med Genet A 155A: 943–968. doi: 10.1002/ajmg.a.33909 21438135

9. O'Driscoll M, Ruiz-Perez VL, Woods CG, Jeggo PA, Goodship JA (2003) A splicing mutation affecting expression of ataxia-telangiectasia and Rad3-related protein (ATR) results in Seckel syndrome. Nat Genet 33: 497–501. 12640452

10. Ogi T, Walker S, Stiff T, Hobson E, Limsirichaikul S, et al. (2012) Identification of the first ATRIP-deficient patient and novel mutations in ATR define a clinical spectrum for ATR-ATRIP Seckel Syndrome. PLoS Genet 8: e1002945. doi: 10.1371/journal.pgen.1002945 23144622

11. Qvist P, Huertas P, Jimeno S, Nyegaard M, Hassan MJ, et al. (2011) CtIP Mutations Cause Seckel and Jawad Syndromes. PLoS Genet 7: e1002310. doi: 10.1371/journal.pgen.1002310 21998596

12. Kalay E, Yigit G, Aslan Y, Brown KE, Pohl E, et al. (2011) CEP152 is a genome maintenance protein disrupted in Seckel syndrome. Nat Genet 43: 23–26. doi: 10.1038/ng.725 21131973

13. Bicknell LS, Bongers EM, Leitch A, Brown S, Schoots J, et al. (2011) Mutations in the pre-replication complex cause Meier-Gorlin syndrome. Nat Genet 43: 356–359. doi: 10.1038/ng.775 21358632

14. Bicknell LS, Walker S, Klingseisen A, Stiff T, Leitch A, et al. (2011) Mutations in ORC1, encoding the largest subunit of the origin recognition complex, cause microcephalic primordial dwarfism resembling Meier-Gorlin syndrome. Nat Genet 43: 350–355. doi: 10.1038/ng.776 21358633

15. de Munnik SA, Bicknell LS, Aftimos S, Al-Aama JY, van Bever Y, et al. (2012) Meier-Gorlin syndrome genotype-phenotype studies: 35 individuals with pre-replication complex gene mutations and 10 without molecular diagnosis. Eur J Hum Genet 20: 598–606. doi: 10.1038/ejhg.2011.269 22333897

16. Guernsey DL, Matsuoka M, Jiang H, Evans S, Macgillivray C, et al. (2011) Mutations in origin recognition complex gene ORC4 cause Meier-Gorlin syndrome. Nat Genet 43: 360–364. doi: 10.1038/ng.777 21358631

17. Al-Dosari MS, Shaheen R, Colak D, Alkuraya FS (2010) Novel CENPJ mutation causes Seckel syndrome. J Med Genet 47: 411–414. doi: 10.1136/jmg.2009.076646 20522431

18. Griffith E, Walker S, Martin CA, Vagnarelli P, Stiff T, et al. (2008) Mutations in pericentrin cause Seckel syndrome with defective ATR-dependent DNA damage signaling. Nat Genet 40: 232–236. 18157127

19. Rauch A, Thiel CT, Schindler D, Wick U, Crow YJ, et al. (2008) Mutations in the pericentrin (PCNT) gene cause primordial dwarfism. Science 319: 816–819. doi: 10.1126/science.1151174 18174396

20. Dauber A, Lafranchi SH, Maliga Z, Lui JC, Moon JE, et al. (2012) Novel microcephalic primordial dwarfism disorder associated with variants in the centrosomal protein ninein. J Clin Endocrinol Metab 97: E2140–2151. doi: 10.1210/jc.2012-2150 22933543

21. Sarig O, Nahum S, Rapaport D, Ishida-Yamamoto A, Fuchs-Telem D, et al. (2012) Short stature, onychodysplasia, facial dysmorphism, and hypotrichosis syndrome is caused by a POC1A mutation. Am J Hum Genet 91: 337–342. doi: 10.1016/j.ajhg.2012.06.003 22840363

22. Shaheen R, Faqeih E, Shamseldin HE, Noche RR, Sunker A, et al. (2012) POC1A truncation mutation causes a ciliopathy in humans characterized by primordial dwarfism. Am J Hum Genet 91: 330–336. doi: 10.1016/j.ajhg.2012.05.025 22840364

23. Stiff T, Alagoz M, Alcantara D, Outwin E, Brunner HG, et al. (2013) Deficiency in origin licensing proteins impairs cilia formation: implications for the aetiology of Meier-Gorlin syndrome. PLoS Genet 9: e1003360. doi: 10.1371/journal.pgen.1003360 23516378

24. He H, Liyanarachchi S, Akagi K, Nagy R, Li J, et al. (2011) Mutations in U4atac snRNA, a component of the minor spliceosome, in the developmental disorder MOPD I. Science 332: 238–240. doi: 10.1126/science.1200587 21474760

25. Edery P, Marcaillou C, Sahbatou M, Labalme A, Chastang J, et al. (2011) Association of TALS developmental disorder with defect in minor splicing component U4atac snRNA. Science 332: 240–243. doi: 10.1126/science.1202205 21474761

26. Cha KB, Karolyi IJ, Hunt A, Wenglikowski AM, Wilkinson JE, et al. (2004) Skeletal dysplasia and male infertility locus on mouse chromosome 9. Genomics 83: 951–960. 15177549

27. Goodier JL, Ostertag EM, Du K, Kazazian HH Jr. (2001) A novel active L1 retrotransposon subfamily in the mouse. Genome Res 11: 1677–1685. 11591644

28. Nellaker C, Keane TM, Yalcin B, Wong K, Agam A, et al. (2012) The genomic landscape shaped by selection on transposable elements across 18 mouse strains. Genome Biol 13: R45. doi: 10.1186/gb-2012-13-6-r45 22703977

29. Beck CR, Garcia-Perez JL, Badge RM, Moran JV (2011) LINE-1 elements in structural variation and disease. Annu Rev Genomics Hum Genet 12: 187–215. doi: 10.1146/annurev-genom-082509-141802 21801021

30. Feng Q, Moran JV, Kazazian HH Jr., Boeke JD (1996) Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 87: 905–916. 8945517

31. Rondeau G, Moreau I, Bezieau S, Petit JL, Heilig R, et al. (2001) Comprehensive analysis of a large genomic sequence at the putative B-cell chronic lymphocytic leukaemia (B-CLL) tumour suppresser gene locus. Mutat Res 458: 55–70. 11691637

32. Morrish TA, Gilbert N, Myers JS, Vincent BJ, Stamato TD, et al. (2002) DNA repair mediated by endonuclease-independent LINE-1 retrotransposition. Nat Genet 31: 159–165. 12006980

33. Jurka J (1997) Sequence patterns indicate an enzymatic involvement in integration of mammalian retroposons. Proc Natl Acad Sci U S A 94: 1872–1877. 9050872

34. Wang Y, Jiang F, Zhuo Z, Wu XH, Wu YD (2013) A method for WD40 repeat detection and secondary structure prediction. PLoS One 8: e65705. doi: 10.1371/journal.pone.0065705 23776530

35. Wu XH, Wang Y, Zhuo Z, Jiang F, Wu YD (2012) Identifying the hotspots on the top faces of WD40-repeat proteins from their primary sequences by beta-bulges and DHSW tetrads. PLoS One 7: e43005. doi: 10.1371/journal.pone.0043005 22916195

36. Van Keuren ML, Gavrilina GB, Filipiak WE, Zeidler MG, Saunders TL (2009) Generating transgenic mice from bacterial artificial chromosomes: transgenesis efficiency, integration and expression outcomes. Transgenic Res 18: 769–785. doi: 10.1007/s11248-009-9271-2 19396621

37. Behringer R, Gertsenstein M, Nagy KV, Nagy A (2014) Manipulating the Mouse Embryo. A laboratory manual. NY: Cold Spring Harbor Press.

38. Manandhar G, Simerly C, Salisbury JL, Schatten G (1999) Centriole and centrin degeneration during mouse spermiogenesis. Cell Motil Cytoskeleton 43: 137–144. 10379838

39. Avasthi P, Scheel JF, Ying G, Frederick JM, Baehr W, et al. (2013) Germline deletion of Cetn1 causes infertility in male mice. J Cell Sci 126: 3204–3213. doi: 10.1242/jcs.128587 23641067

40. Escalier D (2002) Genetic approach to male meiotic division deficiency: the human macronuclear spermatozoa. Mol Hum Reprod 8: 1–7. 11756563

41. Gonczy P (2012) Towards a molecular architecture of centriole assembly. Nat Rev Mol Cell Biol 13: 425–435. doi: 10.1038/nrm3373 22691849

42. May-Simera HL, Kelley MW (2012) Cilia, Wnt signaling, and the cytoskeleton. Cilia 1: 7. doi: 10.1186/2046-2530-1-7 23351924

43. Kuss P, Kraft K, Stumm J, Ibrahim D, Vallecillo-Garcia P, et al. (2014) Regulation of cell polarity in the cartilage growth plate and perichondrium of metacarpal elements by HOXD13 and WNT5A. Dev Biol 385: 83–93. doi: 10.1016/j.ydbio.2013.10.013 24161848

44. Ascenzi MG, Blanco C, Drayer I, Kim H, Wilson R, et al. (2011) Effect of localization, length and orientation of chondrocytic primary cilium on murine growth plate organization. J Theor Biol 285: 147–155. doi: 10.1016/j.jtbi.2011.06.016 21723296

45. de Andrea CE, Wiweger M, Prins F, Bovee JV, Romeo S, et al. (2010) Primary cilia organization reflects polarity in the growth plate and implies loss of polarity and mosaicism in osteochondroma. Lab Invest 90: 1091–1101. doi: 10.1038/labinvest.2010.81 20421870

46. Jakob S, Lovell-Badge R (2011) Sex determination and the control of Sox9 expression in mammals. FEBS J 278: 1002–1009. doi: 10.1111/j.1742-4658.2011.08029.x 21281448

47. Costoya JA, Hobbs RM, Barna M, Cattoretti G, Manova K, et al. (2004) Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 36: 653–659. 15156143

48. Yang QE, Racicot KE, Kaucher AV, Oatley MJ, Oatley JM (2013) MicroRNAs 221 and 222 regulate the undifferentiated state in mammalian male germ cells. Development 140: 280–290. doi: 10.1242/dev.087403 23221369

49. Oatley JM, Brinster RL (2008) Regulation of spermatogonial stem cell self-renewal in mammals. Annu Rev Cell Dev Biol 24: 263–286. doi: 10.1146/annurev.cellbio.24.110707.175355 18588486

50. Brinster CJ, Ryu BY, Avarbock MR, Karagenc L, Brinster RL, et al. (2003) Restoration of fertility by germ cell transplantation requires effective recipient preparation. Biol Reprod 69: 412–420. 12672656

51. Hertel KJ (2008) Combinatorial control of exon recognition. J Biol Chem 283: 1211–1215. 18024426

52. Luan DD, Korman MH, Jakubczak JL, Eickbush TH (1993) Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell 72: 595–605. 7679954

53. Cost GJ, Feng Q, Jacquier A, Boeke JD (2002) Human L1 element target-primed reverse transcription in vitro. EMBO J 21: 5899–5910. 12411507

54. Wei W, Gilbert N, Ooi SL, Lawler JF, Ostertag EM, et al. (2001) Human L1 retrotransposition: cis preference versus trans complementation. Mol Cell Biol 21: 1429–1439. 11158327

55. Esnault C, Maestre J, Heidmann T (2000) Human LINE retrotransposons generate processed pseudogenes. Nat Genet 24: 363–367. 10742098

56. Garcia-Perez JL, Doucet AJ, Bucheton A, Moran JV, Gilbert N (2007) Distinct mechanisms for trans-mediated mobilization of cellular RNAs by the LINE-1 reverse transcriptase. Genome Res 17: 602–611. 17416749

57. Parker HG, VonHoldt BM, Quignon P, Margulies EH, Shao S, et al. (2009) An expressed fgf4 retrogene is associated with breed-defining chondrodysplasia in domestic dogs. Science 325: 995–998. doi: 10.1126/science.1173275 19608863

58. de Boer M, van Leeuwen K, Geissler J, Weemaes CM, van den Berg TK, et al. (2014) Primary Immunodeficiency Caused by an Exonized Retroposed Gene Copy Inserted in the CYBB Gene. Hum Mutat 35: 486–496. doi: 10.1002/humu.22519 24478191

59. Cooke SL, Shlien A, Marshall J, Pipinikas CP, Martincorena I, et al. (2014) Processed pseudogenes acquired somatically during cancer development. Nat Commun 5: 3644. doi: 10.1038/ncomms4644 24714652

60. Vitre BD, Cleveland DW (2012) Centrosomes, chromosome instability (CIN) and aneuploidy. Curr Opin Cell Biol 24: 809–815. doi: 10.1016/j.ceb.2012.10.006 23127609

61. Keller LC, Geimer S, Romijn E, Yates J 3rd, Zamora I, et al. (2009) Molecular architecture of the centriole proteome: the conserved WD40 domain protein POC1 is required for centriole duplication and length control. Mol Biol Cell 20: 1150–1166. doi: 10.1091/mbc.E08-06-0619 19109428

62. Venoux M, Tait X, Hames RS, Straatman KR, Woodland HR, et al. (2013) Poc1A and Poc1B act together in human cells to ensure centriole integrity. J Cell Sci 126: 163–175. doi: 10.1242/jcs.111203 23015594

63. Pearson CG, Osborn DP, Giddings TH Jr., Beales PL, Winey M (2009) Basal body stability and ciliogenesis requires the conserved component Poc1. J Cell Biol 187: 905–920. doi: 10.1083/jcb.200908019 20008567

64. Romereim SM, Conoan NH, Chen B, Dudley AT (2014) A dynamic cell adhesion surface regulates tissue architecture in growth plate cartilage. Development 141: 2085–2095. doi: 10.1242/dev.105452 24764078

65. Berbari NF, O'Connor AK, Haycraft CJ, Yoder BK (2009) The primary cilium as a complex signaling center. Curr Biol 19: R526–535. doi: 10.1016/j.cub.2009.05.025 19602418

66. Singla V, Reiter JF (2006) The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 313: 629–633. 16888132

67. Tummala P, Arnsdorf EJ, Jacobs CR (2010) The Role of Primary Cilia in Mesenchymal Stem Cell Differentiation: A Pivotal Switch in Guiding Lineage Commitment. Cell Mol Bioeng 3: 207–212. 20823950

68. Rais Y, Reich A, Simsa-Maziel S, Moshe M, Idelevich A, et al. (2015) The growth plate's response to load is partially mediated by mechano-sensing via the chondrocytic primary cilium. Cell Mol Life Sci 72: 597–615. doi: 10.1007/s00018-014-1690-4 25084815

69. Shao YY, Wang L, Welter JF, Ballock RT (2012) Primary cilia modulate Ihh signal transduction in response to hydrostatic loading of growth plate chondrocytes. Bone 50: 79–84. doi: 10.1016/j.bone.2011.08.033 21930256

70. de Rooij DG, de Boer P (2003) Specific arrests of spermatogenesis in genetically modified and mutant mice. Cytogenet Genome Res 103: 267–276. 15051947

71. Vogl AW, Vaid KS, Guttman JA (2008) The Sertoli cell cytoskeleton. Adv Exp Med Biol 636: 186–211. doi: 10.1007/978-0-387-09597-4_11 19856169

72. Oatley JM, Brinster RL (2012) The germline stem cell niche unit in mammalian testes. Physiol Rev 92: 577–595. doi: 10.1152/physrev.00025.2011 22535892

73. Beck BB, Phillips JB, Bartram MP, Wegner J, Thoenes M, et al. (2014) Mutation of POC1B in a severe syndromic retinal ciliopathy. Hum Mutat 35: 1153–1162. doi: 10.1002/humu.22618 25044745

74. Roosing S, Lamers IJ, de Vrieze E, van den Born LI, Lambertus S, et al. (2014) Disruption of the basal body protein POC1B results in autosomal-recessive cone-rod dystrophy. Am J Hum Genet 95: 131–142. doi: 10.1016/j.ajhg.2014.06.012 25018096

75. Geister KA, Brinkmeier ML, Hsieh M, Faust SM, Karolyi IJ, et al. (2013) A novel loss-of-function mutation in Npr2 clarifies primary role in female reproduction and reveals a potential therapy for acromesomelic dysplasia, Maroteaux type. Hum Mol Genet 22: 345–357. doi: 10.1093/hmg/dds432 23065701

76. Meganck JA, Kozloff KM, Thornton MM, Broski SM, Goldstein SA (2009) Beam hardening artifacts in micro-computed tomography scanning can be reduced by X-ray beam filtration and the resulting images can be used to accurately measure BMD. Bone 45: 1104–1116. doi: 10.1016/j.bone.2009.07.078 19651256

77. Oatley JM, Brinster RL (2006) Spermatogonial stem cells. Methods Enzymol 419: 259–282. 17141059

78. Kubota H, Avarbock MR, Brinster RL (2004) Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci U S A 101: 16489–16494. 15520394