Germline variants in the SEMA4A gene predispose to familial colorectal cancer type X

Nature Communications

Volumn 5, Issue , 2014, Pages

  Schulz, Eduard ^a   Klampfl, Petra ^a,b   Holzapfel, Stefanie ^c   Janecke, Andreas R ^d   Ulz, Peter ^a   Renner, Wilfried ^a   Kashofer, Karl ^a   Nojima, Satoshi ^e,f   Leitner, Anita ^a   Zebisch, Armin ^a   Wölfler, Albert ^a   Hofer, Sybille ^a   Gerger, Armin ^a   Lax, Sigurd ^g   Beham Schmid, Christine ^a   Steinke, Verena ^c   Heitzer, Ellen ^a   Geigl, Jochen B ^a   Windpassinger, Christian ^a   Hoefler, Gerald ^a   Speicher, Michael R ^a   Richard Boland, C ^h   Kumanogoh, Atsushi ^e,f,i   Sill, Heinz ^a   more..

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

^b General Hospital Graz West   (Austria)

^c UNIVERSITY OF BONN   (Germany)

^d INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^e OSAKA UNIVERSITY   (Japan)

^f OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^g Department of IT and Telecommunications   (Austria)

^h BAYLOR UNIVERSITY MEDICAL CENTER   (United States)

ⁱ JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; SEMA4A PROTEIN; UNCLASSIFIED DRUG; PEDILSTATIN; PHORBOL DERIVATIVE; SEMA4A PROTEIN, HUMAN; SEMAPHORIN;

CANCER; GENE EXPRESSION; GENOMICS; GERM CELL; HERITABILITY; MUTATION; POLYMORPHISM; SIGNALING;

ADULT; AGED; ARTICLE; AUSTRIAN; CANCER GENETICS; CANCER RISK; CANCER SUSCEPTIBILITY; CELL CYCLE PROGRESSION; COHORT ANALYSIS; CONTROLLED STUDY; FAMILIAL COLORECTAL CANCER TYPE X; FEMALE; GENETIC VARIABILITY; GERMLINE MUTATION; HEREDITARY COLORECTAL CANCER; HUMAN; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; PEDIGREE ANALYSIS; PHENOTYPE; SINGLE NUCLEOTIDE POLYMORPHISM; SOMATIC MUTATION; WILD TYPE; AMINO ACID SEQUENCE; CHEMISTRY; COLORECTAL TUMOR; GENETIC PREDISPOSITION; GENETICS; GERM CELL; METABOLISM; MISSENSE MUTATION; MOLECULAR GENETICS; SEQUENCE ALIGNMENT;

AUSTRIA;

ADULT; AGED; AMINO ACID SEQUENCE; COLORECTAL NEOPLASMS; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENETIC VARIATION; GERM CELLS; HUMANS; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PHORBOLS; SEMAPHORINS; SEQUENCE ALIGNMENT;

EID: 84923116889     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6191     Document Type: Article

References (51)

1. Siegel, R., Desantis, C. & Jemal, A. Colorectal cancer statistics, 2014. CA-Cancer. J. Clin. 64, 104-117 (2014).
2. Jasperson, K. W., Tuohy, T. M., Neklason, D. W. & Burt, R. W. Hereditary and familial colon cancer. Gastroenterology 138, 2044-2058 (2010).
3. Lynch, H. T. et al. Review of the Lynch syndrome: history, molecular genetics, screening, differential diagnosis, and medicolegal ramifications. Clin. Genet. 76, 1-18 (2009).
4. Umar, A., Risinger, J. I., Hawk, E. T. & Barrett, J. C. Testing guidelines for hereditary non-polyposis colorectal cancer. Nat. Rev. Cancer 4, 153-158 (2004).
5. Lindor, N. M. et al. Lower cancer incidence in Amsterdam-I criteria families without mismatch repair deficiency: familial colorectal cancer type X. JAMA 293, 1979-1985 (2005).
6. Steinke, V. et al. Evaluating the performance of clinical criteria for predicting mismatch repair gene mutations in Lynch syndrome: A comprehensive analysis of 3671 families. Int. J. Cancer 135, 69-77 (2014).
7. Lindor, N. M. Familial colorectal cancer type X: The other half of hereditary nonpolyposis colon cancer syndrome. Surg. Oncol. Clin. N. Am. 18, 637-645 (2009).
8. Mueller-Koch, Y. et al. Hereditary non-polyposis colorectal cancer: clinical and molecular evidence for a new entity of hereditary colorectal cancer. Gut. 54, 1733-1740 (2005).
9. Engel, C. et al. Risks of less common cancers in proven mutation carriers with lynch syndrome. J. Clin. Oncol. 30, 4409-4415 (2012).
10. Schulz, E. et al. Germline mutations in the DNA damage response genes BRCA1, BRCA2, BARD1 and TP53 in patients with therapy related myeloid neoplasms. J. Med. Genet. 49, 422-428 (2012).
11. Sill, H., Olipitz, W., Zebisch, A., Schulz, E. & Wolfler, A. Therapy-related myeloid neoplasms: pathobiology and clinical characteristics. Br. J. Pharmacol. 162, 792-805 (2011).
12. Farrington, S. M. et al. Germline susceptibility to colorectal cancer due to baseexcision repair gene defects. Am. J. Hum. Genet. 77, 112-119 (2005).
13. Yurgelun, M. B. et al. Microsatellite instability and DNA mismatch repair protein deficiency in Lynch syndrome colorectal polyps. Cancer Prev. Res. (Phila) 5, 574-582 (2012).
14. Kumanogoh, A. et al. Nonredundant roles of Sema4A in the immune system: defective T cell priming and Th1/Th2 regulation in Sema4A-deficient mice. Immunity 22, 305-316 (2005).
15. Delgoffe, G. M. et al. Stability and function of regulatory T cells is maintained by a neuropilin-1-semaphorin-4a axis. Nature 501, 252-256 (2013).
16. Toyofuku, T. et al. Semaphorin-4A, an activator for T-cell-mediated immunity, suppresses angiogenesis via Plexin-D1. EMBO J. 26, 1373-1384 (2007).
17. Abid, A., Ismail, M., Mehdi, S. Q. & Khaliq, S. Identification of novel mutations in the SEMA4A gene associated with retinal degenerative diseases. J. Med. Genet. 43, 378-381 (2006).
18. Nojima, S. et al. A point mutation in Semaphorin 4A associates with defective endosomal sorting and causes retinal degeneration. Nat. Commun. 4, 1406 (2013).
19. Cancer Genome Atlas Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature 487, 330-337 (2012).
20. Mendoza, M. C., Er, E. E. & Blenis, J. The Ras-ERK and PI3K-mTOR pathways: cross-talk and compensation. Trends Biochem. Sci. 36, 320-328 (2011).
21. Shtivelman, E., Sussman, J. & Stokoe, D. A role for PI 3-kinase and PKB activity in the G2/M phase of the cell cycle. Curr. Biol. 12, 919-924 (2002).
22. Shinohara, M., Mikhailov, A. V., Aguirre-Ghiso, J. A. & Rieder, C. L. Extracellular signal-regulated kinase 1/2 activity is not required in mammalian cells during late G2 for timely entry into or exit from mitosis. Mol. Biol. Cell 17, 5227-5240 (2006).
23. Bahadori, B. et al. Polymorphisms of the hypoxia-inducible factor 1 gene and peripheral artery disease. Vasc. Med. 15, 371-374 (2010).
24. Rehman, M. & Tamagnone, L. Semaphorins in cancer: biological mechanisms and therapeutic approaches. Semin. Cell Dev. Biol. 24, 179-189 (2013).
25. Alexandrov, L. B. et al. Signatures of mutational processes in human cancer. Nature 500, 415-421 (2013).
26. Neufeld, G., Sabag, A. D., Rabinovicz, N. & Kessler, O. Semaphorins in angiogenesis and tumor progression. Cold Spring Harb. Perspect. Med. 2, a006718 (2012).
27. Janssen, B. J. et al. Structural basis of semaphorin-plexin signalling. Nature 467, 1118-1122 (2010).
28. Nogi, T. et al. Structural basis for semaphorin signalling through the plexin receptor. Nature 467, 1123-1127 (2010).
29. Croitoru, M. E. et al. Association between biallelic and monoallelic germline MYH gene mutations and colorectal cancer risk. J. Natl Cancer Inst. 96, 1631-1634 (2004).
30. Win, A. K. et al. Risk of colorectal cancer for carriers of mutations in MUTYH, with and without a family history of cancer. Gastroenterology 146, 1208-11. e1-5 (2014).
31. Webb, E. L., Rudd, M. F. & Houlston, R. S. Colorectal cancer risk in monoallelic carriers of MYH variants. Am. J. Hum. Genet. 79, 768-771 author reply 771-2 (2006).
32. Olschwang, S., Blanche, H., de Moncuit, C. & Thomas, G. Similar colorectal cancer risk in patients with monoallelic and biallelic mutations in the MYH gene identified in a population with adenomatous polyposis. Genet. Test. 11, 315-320 (2007).
33. Ismail, M., Abid, A., Anwar, K., Mehdi, S. Q. & Khaliq, S. Refinement of the locus for autosomal recessive cone-rod dystrophy (CORD8) linked to chromosome 1q23-q24 in a Pakistani family and exclusion of candidate genes. J. Hum. Genet. 51, 827-831 (2006).
34. Rice, D. S. et al. Severe retinal degeneration associated with disruption of semaphorin 4A. Invest. Ophthalmol. Vis. Sci. 45, 2767-2777 (2004).
35. Baker, S. M. et al. Enhanced intestinal adenomatous polyp formation in Pms2-;Min mice. Cancer Res. 58, 1087-1089 (1998).
36. Takaku, K. et al. Intestinal tumorigenesis in compound mutant mice of both Dpc4 (Smad4) and Apc genes. Cell 92, 645-656 (1998).
37. Vogelstein, B. et al. Cancer genome landscapes. Science 339, 1546-1558 (2013).
38. Middeldorp, A. et al. Increased frequency of 20q gain and copy-neutral loss of heterozygosity in mismatch repair proficient familial colorectal carcinomas. Int. J. Cancer 130, 837-846 (2012).
39. Luchino, J. et al. Semaphorin 3E suppresses tumor cell death triggered by the plexin D1 dependence receptor in metastatic breast cancers. Cancer Cell 24, 673-685 (2013).
40. Sanchez-de-Abajo, A. et al. Molecular analysis of colorectal cancer tumors from patients with mismatch repair proficient hereditary nonpolyposis colorectal cancer suggests novel carcinogenic pathways. Clin. Cancer Res. 13, 5729-5735 (2007).
41. Francisco, I. et al. Familial colorectal cancer type X syndrome: Two distinct molecular entities? Fam. Cancer 10, 623-631 (2011).
42. Dominguez-Valentin, M., Therkildsen, C., Da Silva, S. & Nilbert, M. Familial colorectal cancer type X: genetic profiles and phenotypic features. Mod. Pathol. doi:10. 1038/modpathol. 2014. 49 (2014).
43. Abecasis, G. R., Cherny, S. S., Cookson, W. O. & Cardon, L. R. Merlin-rapid analysis of dense genetic maps using sparse gene flow trees. Nat. Genet. 30, 97-101 (2002).
44. Ruschendorf, F. & Nurnberg, P. ALOHOMORA: A tool for linkage analysis using 10K SNP array data. Bioinformatics 21, 2123-2125 (2005).
45. Li, H. & Durbin, R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26, 589-595 (2010).
46. DePristo, M. A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491-498 (2011).
47. Wang, K., Li, M. & Hakonarson, H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 38, e164 (2010).
48. Beillard, E. et al. Evaluation of candidate control genes for diagnosis and residual disease detection in leukemic patients using 'real-time' quantitative reverse-transcriptase polymerase chain reaction (RQ-PCR)-a Europe against cancer program. Leukemia 17, 2474-2486 (2003).
49. Rodriguez, S., Gaunt, T. R. & Day, I. N. Hardy-Weinberg equilibrium testing of biological ascertainment for Mendelian randomization studies. Am. J. Epidemiol. 169, 505-514 (2009).
50. Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin) 6, 80-92 (2012).
51. Kelley, L. A. & Sternberg, M. J. Protein structure prediction on the Web: A case study using the Phyre server. Nat. Protoc. 4, 363-371 (2009).