Embryonic left-right separation mechanism allows confinement of mutation-induced phenotypes to one lateral body half of bilaterians

American Journal of Medical Genetics, Part A

Volumn 161, Issue 12, 2013, Pages 3095-3114

  Ma, Kun ^a  

^a NONE   (United States)

Author keywords

Bilateral cancer; CHILD syndrome; Discordant twins; Embryogenesis; Embryonic development; Embryonic left right separation mechanism; Fluctuation asymmetry; Gynandromorph; Gynandromorphism; Hemiatrophy; Left right asymmetry; Unilateral cancer; Unilateral diseases

Indexed keywords

ARTICLE; BILATERIA; BREAST CANCER; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EPIGENETICS; FAMILIAL CANCER; FEMALE; GENE MUTATION; GENETIC DISORDER; HETEROZYGOTE; HUMAN; MALE; MONOZYGOTIC TWINS; MOSAICISM; NONHUMAN; PHENOTYPE; PRIMARY TUMOR; PRIORITY JOURNAL; PROGENY; TWIN DISCORDANCE;

ANIMALIA; BILATERIA;

BILATERAL CANCER; CHILD SYNDROME; DISCORDANT TWINS; EMBRYOGENESIS; EMBRYONIC DEVELOPMENT; EMBRYONIC LEFT-RIGHT SEPARATION MECHANISM; FLUCTUATION ASYMMETRY; GYNANDROMORPH; GYNANDROMORPHISM; HEMIATROPHY; LEFT-RIGHT ASYMMETRY; UNILATERAL CANCER; UNILATERAL DISEASES;

ANIMALS; BODY PATTERNING; BREAST NEOPLASMS; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC DISEASES, INBORN; HUMANS; MUTATION; PHENOTYPE;

EID: 84888023940     PISSN: 15524825     EISSN: 15524833     Source Type: Journal    
DOI: 10.1002/ajmg.a.36188     Document Type: Article

References (127)

1. Agate RJ, Grisham W, Wade J, Mann S, Wingfield J, Schanen C, Palotie A, Arnold AP. 2003. Neural, not gonadal, origin of brain sex differences in a gynandromorphic finch. Proc Natl Acad Sci USA 100:4873-4878.
2. Aknin C, Allart JF, Rouland JF. 2007. Unilateral keratoconus and mirror image in a pair of monozygotic twins. J Fr Ophtalmol 30:899-902.
3. Amos CI, Xu W, Spitz MR. 1999. Is there a genetic basis for lung cancer susceptibility? Recent Results Cancer Res 151:3-12.
4. Anand P, Kunnumakkara AB, Sundaram C, Harikumar KB, Tharakan ST, Lai OS, Sung B, Aggarwal BB. 2008. Cancer is a preventable disease that requires major lifestyle changes. Pharm Res 25:2097-2116.
5. Anderson DE. 1974. Genetic study of breast cancer: Identification of a high risk group. Cancer 34:1090-1097.
6. Armakolas A, Koutsilieris M, Klar AJ. 2010. Discovery of the mitotic selective chromatid segregation phenomenon and its implications for vertebrate development. Curr Opin Cell Biol 22:81-87.
7. Aw S, Levin M. 2008. What's left in asymmetry? Dev Dyn 237:3453-3463.
8. Baptista AP, Cortesao JM. 1979. [Inflammatory variable epidermal naevus (atypical I.L.V.E.N.? A new entity?) (author's transl)]. Ann Dermatol Venereol 106:443-450.
9. Baranzini SE, Mudge J, van Velkinburgh JC, Khankhanian P, Khrebtukova I, Miller NA, Zhang L, Farmer AD, Bell CJ, Kim RW, et al. 2010. Genome, epigenome and RNA sequences of monozygotic twins discordant for multiple sclerosis. Nature 464:1351-1356.
10. Berger-Zaslav AL, Mehta L, Jacob J, Mercado T, Gadi I, Tepperberg JH, Palmer LS. 2009. Ovotesticular disorder of sexual development (true hermaphroditism). Urology 73:293-296.
11. Beyan H, Drexhage RC, van der Heul Nieuwenhuijsen L, de Wit H, Padmos RC, Schloot NC, Drexhage HA, Leslie RD. 2010. Monocyte gene-expression profiles associated with childhood-onset type 1 diabetes and disease risk: A study of identical twins. Diabetes 59:1751-1755.
12. Bieber FR, Nance WE, Morton CC, Brown JA, Redwine FO, Jordan RL, Mohanakumar T. 1981. Genetic studies of an acardiac monster: Evidence of polar body twinning in man. Science 213:775-777.
13. Bittar M, Happle R, Grzeschik KH, Leveleki L, Hertl M, Bornholdt D, König A. 2006. CHILD syndrome in 3 generations: The importance of mild or minimal skin lesions. Arch Dermatol 142:348-351.
14. Bliek J, Alders M, Maas SM, Oostra RJ, Mackay DM, van der Lip K, Callaway JL, Brooks A, van't Padje S, Westerveld A, et al. 2009. Lessons from BWS twins: Complex maternal and paternal hypomethylation and a common source of haematopoietic stem cells. Eur J Hum Genet 17:1625-1634.
15. Bornholdt D, König A, Happle R, Leveleki L, Bittar M, Danarti R, Vahlquist A, Tilgen W, Reinhold U, Poiares BA, et al. 2005. Mutational spectrum of NSDHL in CHILD syndrome. J Med Genet 42:e17.
16. Caporaso NE. 2002. Why have we failed to find the low penetrance genetic constituents of common cancers? Cancer Epidemiol Biomarkers Prev 11:1544-1549.
17. Cardno AG, Gottesman II. 2000. Twin studies of schizophrenia: From bow-and-arrow concordances to star wars Mx and functional genomics. Am J Med Genet 97:12-17.
18. Chen Y, Thompson W, Semenciw R, Mao Y. 1999. Epidemiology of contralateral breast cancer. Cancer Epidemiol Biomarkers Prev 8:855-861.
19. Cidis MB, Warshowsky JH, Goldrich SG, Meltzer CC. 1997. Mirror-image optic nerve dysplasia with associated anisometropia in identical twins. J Am Optom Assoc 68:325-329.
20. Cloos J, Nieuwenhuis EJ, Boomsma DI, Kuik DJ, van der Sterre ML, Arwert F, Snow GB, Braakhuis BJ. 1999. Inherited susceptibility to bleomycin-induced chromatid breaks in cultured peripheral blood lymphocytes. J Natl Cancer Inst 91:1125-1130.
21. Conboy IM, Rando TA. 2002. The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev Cell 3:397-409.
22. Costa T, Lambert M, Teshima I, Ray PN, Richer CL, Dallaire L. 1998. Monozygotic twins with 45, X/46, XY mosaicism discordant for phenotypic sex. Am J Med Genet 75:40-44.
23. Cunningham D, Spychala K, McLarren KW, Garza LA, Boerkoel CF, Herman GE. 2009. Developmental expression pattern of the cholesterogenic enzyme NSDHL and negative selection of NSDHL-deficient cells in the heterozygous Bpa(1H)/+ mouse. Mol Genet Metab 98:356-366.
24. Danarti R, Grzeschik KH, Radiono S, König A, Happle R. 2010. Left-sided CHILD syndrome caused by a nonsense mutation in exon 7 of the NSDHL gene. Eur J Dermatol 20:634-635.
25. Danilchik MV, Black SD. 1988. The first cleavage plane and the embryonic axis are determined by separate mechanisms in Xenopus laevis. I. Independence in undisturbed embryos. Dev Biol 128:58-64.
26. Danos MC, Yost HJ. 1996. Role of notochord in specification of cardiac left-right orientation in zebrafish and Xenopus. Dev Biol 177:96-103.
27. Djaldetti R, Ziv I, Melamed E. 2006. The mystery of motor asymmetry in Parkinson's disease. Lancet Neurol 5:796-802.
28. Eyal-Giladi H, Kochav S. 1976. From cleavage to primitive streak formation: A complementary normal table and a new look at the first stages of the development of the chick. I. General morphology. Dev Biol 49:321-337.
29. Finch GD, Dawe CJ. 2003. Hemiatrophy. J Pediatr Orthop 23:99-101.
30. Forman D, Oliver RT, Brett AR, Marsh SG, Moses JH, Bodmer JG, Chilvers CE, Pike MC. 1992. Familial testicular cancer: A report of the UK family register, estimation of risk and an HLA class 1 sib-pair analysis. Br J Cancer 65:255-262.
31. Fossa SD, Chen J, Schonfeld SJ, McGlynn KA, McMaster ML, Gail MH, Travis LB. 2005. Risk of contralateral testicular cancer: A population-based study of 29, 515 U.S. men. J Natl Cancer Inst 97:1056-1066.
32. Fuentealba LC, Eivers E, Geissert D, Taelman V, De Robertis EM. 2008. Asymmetric mitosis: Unequal segregation of proteins destined for degradation. Proc Natl Acad Sci USA 105:7732-7737.
33. Fujii T, Shimada T. 2007. Sex determination in the silkworm, Bombyx mori: A female determinant on the W chromosome and the sex-determining gene cascade. Semin Cell Dev Biol 18:379-388.
34. Fujimori T, Kurotaki Y, Miyazaki J, Nabeshima Y. 2003. Analysis of cell lineage in two- and four-cell mouse embryos. Development 130:5113-5122.
35. Gardner RL. 2010. Normal bias in the direction of fetal rotation depends on blastomere composition during early cleavage in the mouse. PLoS ONE 5:e9610.
36. Gartler SM, Francke U. 1975. Half chromatid mutations: Transmission in humans? Am J Hum Genet 27:218-223.
37. Gartler SM, Waxman SH, Giblett E. 1962. An XX/XY human hermaphrodite resulting from double fertilization. Proc Natl Acad Sci USA 48:332-335.
38. Ghazani AA, Arneson N, Warren K, Pintilie M, Bayani J, Squire JA, Done SJ. 2007. Genomic alterations in sporadic synchronous primary breast cancer using array and metaphase comparative genomic hybridization. Neoplasia 9:511-520.
39. Gordon L, Joo JE, Powell JE, Ollikainen M, Novakovic B, Li X, Andronikos R, Cruickshank MN, Conneely KN, Smith AK, et al. 2012. Neonatal DNA methylation profile in human twins is specified by a complex interplay between intrauterine environmental and genetic factors, subject to tissue-specific influence. Genome Res 22:1395-1406.
40. Goto T, Nemoto T, Okuma T, Kobayashi H, Funata N. 2008. Mirror-image solitary bone cyst of the humerus in a pair of mirror-image monozygotic twins. Arch Orthop Trauma Surg 128:1403-1406.
41. Grzeschik KH. 2002. Human limb malformations; an approach to the molecular basis of development. Int J Dev Biol 46:983-991.
42. Hall JG. 2003. Twinning. Lancet 362:735-743.
43. Happle R. 1986. The McCune-Albright syndrome: A lethal gene surviving by mosaicism. Clin Genet 29:321-324.
44. Happle R. 1987. Lethal genes surviving by mosaicism: A possible explanation for sporadic birth defects involving the skin. J Am Acad Dermatol 16:899-906.
45. Happle R. 1992. Paradominant inheritance: A possible explanation for Baker's pigmanted hairy nevus. Eur J Dermatol 2:39-40.
46. Happle R. 1993. Mosaicism in human skin. Understanding the patterns and mechanisms. Arch Dermatol 129:1460-1470.
47. Happle R, Koch H, Lenz W. 1980. The CHILD syndrome. Congenital hemidysplasia with ichthyosiform erythroderma and limb defects. Eur J Pediatr 134:27-33.
48. Happle R, Karlic D, Steijlen PM. 1990. [CHILD syndrome in a mother and daughter]. Hautarzt 41:105-108.
49. Happle R, Effendy I, Megahed M, Orlow SJ, Kuster W. 1996. CHILD syndrome in a boy. Am J Med Genet 62:192-194.
50. Hartman M, Czene K, Reilly M, Bergh J, Lagiou P, Trichopoulos D, Adami HO, Hall P. 2005. Genetic implications of bilateral breast cancer: A population based cohort study. Lancet Oncol 6:377-382.
51. Hartman M, Hall P, Edgren G, Reilly M, Lindstrom L, Lichtenstein P, Kaprio J, Skytthe A, Peto J, Czene K. 2008. Breast cancer onset in twins and women with bilateral disease. J Clin Oncol 26:4086-4091.
52. Harvey RP, Melton DA. 1988. Microinjection of synthetic Xhox-1A homeobox mRNA disrupts somite formation in developing Xenopus embryos. Cell 53:687-697.
53. Healey SC, Kirk KM, Hyland VJ, Munns CF, Henders AK, Batch JA, Heath AC, Martin NG, Glass IA. 2001. Height discordance in monozygotic females is not attributable to discordant inactivation of X-linked stature determining genes. Twin Res 4:19-24.
54. Helland CA, Wester K. 2007. Monozygotic twins with mirror image cysts: Indication of a genetic mechanism in arachnoid cysts? Neurology 69:110-111.
55. Hemminki K, Vaittinen P. 1999. Familial risks in second primary breast cancer based on a family cancer database. Eur J Cancer 35:455-458.
56. Hollander WF, Gowen JW, Stadler J. 1956. A study of 25 gynandromorphic mice of the Bagg albino strain. Anat Rec 124:223-243.
57. Hyttinen V, Kaprio J, Kinnunen L, Koskenvuo M, Tuomilehto J. 2003. Genetic liability of type 1 diabetes and the onset age among 22, 650 young Finnish twin pairs: A nationwide follow-up study. Diabetes 52:1052-1055.
58. Jacobson M, Hirose G. 1978. Origin of the retina from both sides of the embryonic brain: A contribution to the problem of crossing at the optic chiasma. Science 202:637-639.
59. Kaminsky ZA, Tang T, Wang SC, Ptak C, Oh GH, Wong AH, Feldcamp LA, Virtanen C, Halfvarson J, Tysk C, et al. 2009. DNA methylation profiles in monozygotic and dizygotic twins. Nat Genet 41:240-245.
60. Kaprio J, Tuomilehto J, Koskenvuo M, Romanov K, Reunanen A, Eriksson J, Stengard J, Kesaniemi YA. 1992. Concordance for type 1 (insulin-dependent) and type 2 (non-insulin-dependent) diabetes mellitus in a population-based cohort of twins in Finland. Diabetologia 35:1060-1067.
61. Kato T, Iwamoto K, Kakiuchi C, Kuratomi G, Okazaki Y. 2005. Genetic or epigenetic difference causing discordance between monozygotic twins as a clue to molecular basis of mental disorders. Mol Psychiatry 10:622-630.
62. Klein SL. 1987. The first cleavage furrow demarcates the dorsal-ventral axis in Xenopus embryos. Dev Biol 120:299-304.
63. Kondo S, Schutte BC, Richardson RJ, Bjork BC, Knight AS, Watanabe Y, Howard E, de Lima RL, Daack-Hirsch S, Sander A, et al. 2002. Mutations in IRF6 cause Van der Woude and popliteal pterygium syndromes. Nat Genet 32:285-289.
64. König A, Happle R, Bornholdt D, Engel H, Grzeschik KH. 2000. Mutations in the NSDHL gene, encoding a 3beta-hydroxysteroid dehydrogenase, cause CHILD syndrome. Am J Med Genet 90:339-346.
65. König A, Happle R, Fink-Puches R, Soyer HP, Bornholdt D, Engel H, Grzeschik KH. 2002. A novel missense mutation of NSDHL in an unusual case of CHILD syndrome showing bilateral, almost symmetric involvement. J Am Acad Dermatol 46:594-596.
66. Kyvik KO, Green A, Beck-Nielsen H. 1995. Concordance rates of insulin dependent diabetes mellitus: A population based study of young Danish twins. BMJ 311:913-917.
67. Lenhart KF, Lin SY, Titus TA, Postlethwait JH, Burdine RD. 2011. Two additional midline barriers function with midline lefty1 expression to maintain asymmetric Nodal signaling during left-right axis specification in zebrafish. Development 138:4405-4410.
68. Letts RM, Shokeir MH. 1975. Mirror-image coxa vara in identical twins. J Bone Joint Surg Am 57:117-118.
69. Levin M, Palmer AR. 2007. Left-right patterning from the inside out: Widespread evidence for intracellular control. Bioessays 29:271-287.
70. Levin M, Pagan S, Roberts DJ, Cooke J, Kuehn MR, Tabin CJ. 1997. Left/right patterning signals and the independent regulation of different aspects of situs in the chick embryo. Dev Biol 189:57-67.
71. Li CC, Chodirker BN, Dawson AJ, Chudley AE. 2004. Severe hemihypotrophy in a female infant with mosaic Turner syndrome: A variant of Russell-Silver syndrome? Clin Dysmorphol 13:95-98.
72. Lichtenstein P, Holm NV, Verkasalo PK, Iliadou A, Kaprio J, Koskenvuo M, Pukkala E, Skytthe A, Hemminki K. 2000. Environmental and heritable factors in the causation of cancer-Analyses of cohorts of twins from Sweden, Denmark, and Finland. N Engl J Med 343:78-85.
73. Liu KJ, Harland RM. 2005. Inhibition of neurogenesis by SRp38, a neuroD-regulated RNA-binding protein. Development 132:1511-1523.
74. Machin GA. 1996. Some causes of genotypic and phenotypic discordance in monozygotic twin pairs. Am J Med Genet 61:216-228.
75. Machin G. 2009. Non-identical monozygotic twins, intermediate twin types, zygosity testing, and the non-random nature of monozygotic twinning: A review. Am J Med Genet Part C 151C:110-127.
76. Marcus DM, Papastergiou GI, Patel M, Pandya A, Brooks SE. 1999. Discordant retinoblastoma in monozygotic twins. Am J Ophthalmol 128:524-526.
77. Marusyk A, Polyak K. 2010. Tumor heterogeneity: Causes and consequences. Biochim Biophys Acta 1805:105-117.
78. Masho R. 1990. Close correlation between the first cleavage plane and the body axis in early Xenopus embryos. Dev Growth Differ 32:57-64.
79. McClellan J, King MC. 2010. Genetic heterogeneity in human disease. Cell 141:210-217.
80. Meinhardt H. 2004. Different strategies for midline formation in bilaterians. Nat Rev Neurosci 5:502-510.
81. Meno C, Shimono A, Saijoh Y, Yashiro K, Mochida K, Ohishi S, Noji S, Kondoh H, Hamada H. 1998. lefty-1 is required for left-right determination as a regulator of lefty-2 and nodal. Cell 94:287-297.
82. Mikawa T, Poh AM, Kelly KA, Ishii Y, Reese DE. 2004. Induction and patterning of the primitive streak, an organizing center of gastrulation in the amniote. Dev Dyn 229:422-432.
83. Morison D, Reyes CV, Skorodin MS. 1994. Mirror-image tumors in mirror-image twins. Chest 106:608-610.
84. Nance WE. 1990. Do twin Lyons have larger spots? Am J Hum Genet 46:646-648.
85. Nicholson PW, Harland SJ. 1995. Inheritance and testicular cancer. Br J Cancer 71:421-426.
86. Nutt SL, Dingwell KS, Holt CE, Amaya E. 2001. Xenopus Sprouty2 inhibits FGF-mediated gastrulation movements but does not affect mesoderm induction and patterning. Genes Dev 15:1152-1166.
87. Okamoto F, Nonoyama T, Hommura S. 2001. Mirror image myopic anisometropia in two pairs of monozygotic twins. Ophthalmologica 215:435-438.
88. Palmer AR. 2009. Animal asymmetry. Curr Biol 19:R473-R477.
89. Papenhausen PR, Mueller OT, Bercu B, Salazar J, Tedesco TA. 1991. Cell line segregation in a 45, X/46, XY mosaic child with asymmetric leg growth. Clin Genet 40:237-241.
90. Perlman EJ, Stetten G, Tuck-Muller CM, Farber RA, Neuman WL, Blakemore KJ, Hutchins GM. 1990. Sexual discordance in monozygotic twins. Am J Med Genet 37:551-557.
91. Petronis A. 2006. Epigenetics and twins: Three variations on the theme. Trends Genet 22:347-350.
92. Poblete-Gutierrez P, Wiederholt T, König A, Jugert FK, Marquardt Y, Rubben A, Merk HF, Happle R, Frank J. 2004. Allelic loss underlies type 2 segmental Hailey-Hailey disease, providing molecular confirmation of a novel genetic concept. J Clin Invest 114:1467-1474.
93. Pohl C, Bao Z. 2010. Chiral forces organize left-right patterning in C. elegans by uncoupling midline and anteroposterior axis. Dev Cell 19:402-412.
94. Raiha I, Kaprio J, Koskenvuo M, Rajala T, Sourander L. 1996. Alzheimer's disease in Finnish twins. Lancet 347:573-578.
95. Rajakulendran S, Kuntzer T, Dunand M, Yau SC, Ashton EJ, Storey H, McCauley J, Abbs S, Thonney F, Leturcq F, et al. 2010. Marked hemiatrophy in carriers of Duchenne muscular dystrophy. Arch Neurol 67:497-500.
96. Richards CS, Watkins SC, Hoffman EP, Schneider NR, Milsark IW, Katz KS, Cook JD, Kunkel LM, Cortada JM. 1990. Skewed X inactivation in a female MZ twin results in Duchenne muscular dystrophy. Am J Hum Genet 46:672-681.
97. Ristori G, Cannoni S, Stazi MA, Vanacore N, Cotichini R, Alfo M, Pugliatti M, Sotgiu S, Solaro C, Bomprezzi R, et al. 2006. Multiple sclerosis in twins from continental Italy and Sardinia: A nationwide study. Ann Neurol 59:27-34.
98. Robertson SP, Thompson S, Morgan T, Holder-Espinasse M, Martinot-Duquenoy V, Wilkie AO, Manouvrier-Hanu S. 2006. Postzygotic mutation and germline mosaicism in the otopalatodigital syndrome spectrum disorders. Eur J Hum Genet 14:549-554.
99. Roychoudhuri R, Putcha V, Moller H. 2006. Cancer and laterality: A study of the five major paired organs (UK). Cancer Causes Control 17:655-662.
100. Sakuntabhai A, Ruiz-Perez V, Carter S, Jacobsen N, Burge S, Monk S, Smith M, Munro CS, O'Donovan M, Craddock N, et al. 1999. Mutations in ATP2A2, encoding a Ca2+ pump, cause Darier disease. Nat Genet 21:271-277.
101. Schwindinger WF, Francomano CA, Levine MA. 1992. Identification of a mutation in the gene encoding the alpha subunit of the stimulatory G protein of adenylyl cyclase in McCune-Albright syndrome. Proc Natl Acad Sci USA 89:5152-5156.
102. Shimotori T, Goto T. 2001. Developmental fates of the first four blastomeres of the chaetognath Paraspadella gotoi: Relationship to protostomes. Dev Growth Differ 43:371-382.
103. Shiratori H, Yashiro K, Shen MM, Hamada H. 2006. Conserved regulation and role of Pitx2 in situs-specific morphogenesis of visceral organs. Development 133:3015-3025.
104. Souter VL, Parisi MA, Nyholt DR, Kapur RP, Henders AK, Opheim KE, Gunther DF, Mitchell ME, Glass IA, Montgomery GW. 2007. A case of true hermaphroditism reveals an unusual mechanism of twinning. Hum Genet 121:179-185.
105. Sperber GH, Machin GA, Bamforth FJ. 1994. Mirror-image dental fusion and discordance in monozygotic twins. Am J Med Genet 51:41-45.
106. Spitz MR, Bondy ML. 1993. Genetic susceptibility to cancer. Cancer 72:991-995.
107. Spitz MR, Wei Q, Dong Q, Amos CI, Wu X. 2003. Genetic susceptibility to lung cancer: The role of DNA damage and repair. Cancer Epidemiol Biomarkers Prev 12:689-698.
108. Strain L, Warner JP, Johnston T, Bonthron DT. 1995. A human parthenogenetic chimaera. Nat Genet 11:164-169.
109. Stratton MR, Campbell PJ, Futreal PA. 2009. The cancer genome. Nature 458:719-724.
110. Summers RG, Piston DW, Harris KM, Morrill JB. 1996. The orientation of first cleavage in the sea urchin embryo, Lytechinus variegatus, does not specify the axes of bilateral symmetry. Dev Biol 175:177-183.
111. Tanner CM, Ottman R, Goldman SM, Ellenberg J, Chan P, Mayeux R, Langston JW. 1999. Parkinson disease in twins: An etiologic study. JAMA 281:341-346.
112. Trousse D, Barlesi F, Loundou A, Tasei AM, Doddoli C, Giudicelli R, Astoul P, Fuentes P, Thomas P. 2007. Synchronous multiple primary lung cancer: An increasing clinical occurrence requiring multidisciplinary management. J Thorac Cardiovasc Surg 133:1193-1200.
113. Vadlamudi L, Dibbens LM, Lawrence KM, Iona X, McMahon JM, Murrell W, Mackay-Sim A, Scheffer IE, Berkovic SF. 2010. Timing of de novo mutagenesis-A twin study of sodium-channel mutations. N Engl J Med 363:1335-1340.
114. Van Dongen S, Sprengers E, Helle S. 2012. Hand asymmetry does not relate to key life history traits in post-menopausal contemporary Finnish women. PLoS ONE 7:e34661.
115. Vandenberg LN, Levin M. 2010a. Consistent left-right asymmetry cannot be established by late organizers in Xenopus unless the late organizer is a conjoined twin. Development 137:1095-1105.
116. Vandenberg LN, Levin M. 2010b. Far from solved: A perspective on what we know about early mechanisms of left-right asymmetry. Dev Dyn 239:3131-3146.
117. Vandenberg LN, Levin M. 2013. A unified model for left-right asymmetry? Comparison and synthesis of molecular models of embryonic laterality. Dev Biol 379:1-15.
118. Weinstein LS, Shenker A, Gejman PV, Merino MJ, Friedman E, Spiegel AM. 1991. Activating mutations of the stimulatory G protein in the McCune-Albright syndrome. N Engl J Med 325:1688-1695.
119. Weksberg R, Shuman C, Caluseriu O, Smith AC, Fei YL, Nishikawa J, Stockley TL, Best L, Chitayat D, Olney A, et al. 2002. Discordant KCNQ1OT1 imprinting in sets of monozygotic twins discordant for Beckwith-Wiedemann syndrome. Hum Mol Genet 11:1317-1325.
120. White MJ, Webb GC, Cheney J. 1973. Cytogenetics of the parthenogenetic grasshopper Moraba virgo and its bisexual relatives. I. A new species of the virgo group with a unique sex chromosome mechanism. Chromosoma 40:199-212.
121. Wiedemann HR, Opitz JM. 1983. Brief clinical report: Unilateral partial tibia defect with preaxial polydactyly, general micromelia, and trigonomacrocephaly with a note on "developmental resistance." Am J Med Genet 14:467-471.
122. Wiklund F, Tretli S, Choueiri TK, Signoretti S, Fall K, Adami HO. 2009. Risk of bilateral renal cell cancer. J Clin Oncol 27:3737-3741.
123. Willer CJ, Dyment DA, Risch NJ, Sadovnick AD, Ebers GC. 2003. Twin concordance and sibling recurrence rates in multiple sclerosis. Proc Natl Acad Sci USA 100:12877-12882.
124. Wu SC, Lin ZQ, Xu CW, Koo KS, Huang OL, Xie DQ. 1987. Multiple primary lung cancers. Chest 92:892-896.
125. Wu X, Gu J, Spitz MR. 2007. Mutagen sensitivity: A genetic predisposition factor for cancer. Cancer Res 67:3493-3495.
126. Zhao D, McBride D, Nandi S, McQueen HA, McGrew MJ, Hocking PM, Lewis PD, Sang HM, Clinton M. 2010. Somatic sex identity is cell autonomous in the chicken. Nature 464:237-242.
127. Zhou JY, Pu JL, Chen S, Hong Y, Ling CH, Zhang JM. 2011. Mirror-image arachnoid cysts in a pair of monozygotic twins: A case report and review of the literature. Int J Med Sci 8:402-405.