A primate-specific acceleration in the evolution of the caspase-dependent apoptosis pathway

Human Molecular Genetics

Volumn 15, Issue 20, 2006, Pages 3034-3040

  Vallender, Eric J ^a   Lahn, Bruce T ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CASPASE; CASPASE 3; CASPASE 9;

AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; BRAIN SIZE; CARNIVORA; CELL COUNT; CONTROLLED STUDY; GENE FUNCTION; GENE IDENTIFICATION; GENE MUTATION; GENETIC ASSOCIATION; GENETIC CODE; GENETIC SELECTION; GENETIC VARIABILITY; GROWTH REGULATION; HUMAN GENETICS; MAMMAL CELL; MOLECULAR EVOLUTION; NERVE CELL; OBSERVATIONAL STUDY; PRIMATE; PRIORITY JOURNAL; RODENT; TAXONOMY;

ANIMALS; APOPTOSIS; APOPTOTIC PROTEASE-ACTIVATING FACTOR 1; BASE SEQUENCE; BRAIN; CARNIVORA; CASPASE 3; CASPASE 9; CASPASES; DATABASES, GENETIC; EVOLUTION, MOLECULAR; HUMANS; NERVOUS SYSTEM; PRIMATES; RODENTIA; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

MAMMALIA; PRIMATES; RODENTIA;

EID: 33749551431     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddl245     Document Type: Article

References (49)

1. Twomey, C. and McCarthy, J.V. (2005) Pathways of apoptosis and importance in development. J. Cell. Mol. Med., 9, 345-359.
2. Clarke, P.G. and Clarke, S. (1996) Nineteenth century research on naturally occurring cell death and related phenomena. Anat. Embryol. (Berl.), 193, 81-99.
3. Jacobson, M.D., Weil, M. and Raff, M.C. (1997) Programmed cell death in animal development. Cell, 88, 347-354.
4. Haydar, T.F., Kuan, C.Y., Flavell, R.A. and Rakic, P. (1999) The role of cell death in regulating the size and shape of the mammalian forebrain. Cereb. Cortex, 9, 621-626.
5. Kuan, C.Y., Roth, K.A., Flavell, R.A. and Rakic, P. (2000) Mechanisms of programmed cell death in the developing brain. Trends Neurosci., 23, 291-297.
6. Putcha, G.V., Harris, C.A., Moulder, K.L., Easton, R.M., Thompson, C.B. and Johnson, E.M., Jr. (2002) Intrinsic and extrinsic pathway signaling during neuronal apoptosis: Lessons from the analysis of mutant mice. J. Cell Biol., 157, 441-453.
7. Lossi, L. and Merighi, A. (2003) In vivo cellular and molecular mechanisms of neuronal apoptosis in the mammalian CNS. Prog. Neurobiol., 69, 287-312.
8. Buss, R.R. and Oppenheim, R.W. (2004) Role of programmed cell death in normal neuronal development and function. Anat. Sci. Int., 79, 191-197.
9. Lossi, L., Cantile, C., Tamagno, I. and Merighi, A. (2005) Apoptosis in the mammalian CNS: Lessons from animal models. Vet. J., 170, 52-66.
10. Rakic, S. and Zecevic, N. (2000) Programmed cell death in the developing human telencephalon. Eur. J. Neurosci., 12, 2721-2734.
11. Chan, W.Y., Lorke, D.E., Tiu, S.C. and Yew, D.T. (2002) Proliferation and apoptosis in the developing human neocortex. Anat. Rec., 267, 261-276.
12. Cecconi, F., Alvarez-Bolado, G., Meyer, B.I., Roth, K.A. and Gruss, P. (1998) Apaf1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell, 94, 727-737.
13. Yoshida, H., Kong, Y.Y., Yoshida, R., Elia, A.J., Hakem, A., Hakem, R., Penninger, J.M. and Mak, T.W. (1998) Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell, 94, 739-750.
14. Honarpour, N., Gilbert, S.L., Lahn, B.T., Wang, X. and Herz, J. (2001) Apaf-1 deficiency and neural tube closure defects are found in fog mice. Proc. Natl Acad. Sci. USA, 98, 9683-9687.
15. Hakem, R., Hakem, A., Duncan, G.S., Henderson, J.T., Woo, M., Soengas, M.S., Elia, A., de la Pompa, J.L., Kagi, D., Khoo, W. et al. (1998) Differential requirement for caspase 9 in apoptotic pathways in vivo. Cell, 94, 339-352.
16. Kuida, K., Haydar, T.F., Kuan, C.Y., Gu, Y., Taya, C., Karasuyama, H., Su, M.S., Rakic, P. and Flavell, R.A. (1998) Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell, 94, 325-337.
17. Kuida, K., Zheng, T.S., Na, S., Kuan, C., Yang, D., Karasuyama, H., Rakic, P. and Flavell, R.A. (1996) Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature, 384, 368-372.
18. Hughes, A.L. (1994) The evolution of functionally novel proteins after gene duplication. Proc. Biol. Sci., 256, 119-124.
19. Force, A., Lynch, M., Pickett, F.B., Amores, A., Yan, Y.L. and Postlethwait, J. (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics, 151, 1531-1545.
20. Li, W.H. (1997) Molecular Evolution, Sinauer Associates, Sunderland, Massachusetts.
21. McDonald, J.H. and Kreitman, M. (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature, 351, 652-654.
22. Bustamante, C.D., Fledel-Alon, A., Williamson, S., Nielsen, R., Hubisz, M.T., Glanowski, S., Tanenbaum, D.M., White, T.J., Sninsky, J.J., Hernandez, R.D. et al. (2005) Natural selection on protein-coding genes in the human genome. Nature, 437, 1153-1157.
23. Budihardjo, I., Oliver, H., Lutter, M., Luo, X. and Wang, X. (1999) Biochemical pathways of caspase activation during apoptosis. Annu. Rev. Cell Dev. Biol., 15, 269-290.
24. Roth, K.A., Kuan, C., Haydar, T.F., D'Sa-Eipper, C., Shindler, K.S., Zheng, T.S., Kuida, K., Flavell, R.A. and Rakic, P. (2000) Epistatic and independent functions of caspase-3 and Bcl-X(L) in developmental programmed cell death. Proc. Natl Acad. Sci. USA, 97, 466-471.
25. Gilbert, S.L., Dobyns, W.B. and Lahn, B.T. (2005) Genetic links between brain development and brain evolution. Nat. Rev. Genet., 6, 581-590.
26. Zhang, J. (2003) Evolution of the human ASPM gene, a major determinant of brain size. Genetics, 165, 2063-2070.
27. Evans, P.D., Anderson, J.R., Vallender, E.J., Gilbert, S.L., Malcom, C.M., Dorus, S. and Lahn, B.T. (2004) Adaptive evolution of ASPM, a major determinant of cerebral cortical size in humans. Hum. Mol. Genet., 13, 489-494.
28. Kouprina, N., Pavlicek, A., Mochida, G.H., Solomon, G., Gersch, W., Yoon, Y.H., Collura, R., Ruvolo, M., Barrett, J.C., Woods, C.G. et al. (2004) Accelerated evolution of the ASPM gene controlling brain size begins prior to human brain expansion. PLoS Biol., 2, E126.
29. Wang, Y.Q. and Su, B. (2004) Molecular evolution of microcephalin, a gene determining human brain size. Hum. Mol. Genet., 13, 1131-1137.
30. Evans, P.D., Anderson, J.R., Vallender, E.J., Choi, S.S. and Lahn, B.T. (2004) Reconstructing the evolutionary history of microcephalin, a gene controlling human brain size. Hum. Mol. Genet., 13, 1139-1145.
31. Dorus, S., Vallender, E.J., Evans, P.D., Anderson, J.R., Gilbert, S.L., Mahowald, M., Wyckoff, G.J., Malcom, C.M. and Lahn, B.T. (2004) Accelerated evolution of nervous system genes in the origin of Homo sapiens. Cell, 119, 1027-1040.
32. Evans, P.D., Gilbert, S.L., Mekel-Bobrov, N., Vallender, E.J., Anderson, J.R., Vaez-Azizi, L.M., Tishkoff, S.A., Hudson, R.R. and Lahn, B.T. (2005) Microcephalin, a gene regulating brain size, continues to evolve adaptively in humans. Science, 309, 1717-1720.
33. Mekel-Bobrov, N., Gilbert, S.L., Evans, P.D., Vallender, E.J., Anderson, J.R., Hudson, R.R., Tishkoff, S.A. and Lahn, B.T. (2005) Ongoing adaptive evolution of ASPM, a brain size determinant in Homo sapiens. Science, 309, 1720-1722.
34. Evans, P.D., Vallender, E.J. and Lahn, B.T. (2006) Molecular evolution of the brain size regulator genes CDK5RAP2 and CENPJ. Gene, 375, 75-79.
35. Pavlicek, A. and Jurka, J. (2006) Positive selection on the nonhomologous end-joining factor Cernunnos-XLF in the human lineage. Biol. Direct., 1, 15.
36. Dorus, S., Anderson, J.R., Vallender, E.J., Gilbert, S.L., Zhang, L., Chemnick, L.G., Ryder, O.A., Li, W. and Lahn, B.T. (2006) Sonic Hedgehog, a key development gene, experienced intensified molecular evolution in primates. Hum. Mol. Genet., 15, 2031-2037.
37. Hu, Y., Ding, L., Spencer, D.M. and Nunez, G. (1998) WD-40 repeat region regulates Apaf-1 self-association and procaspase-9 activation. J. Biol. Chem., 273, 33489-33494.
38. Benedict, M.A., Hu, Y., Inohara, N. and Nunez, G. (2000) Expression and functional analysis of Apaf-1 isoforms. Extra Wd-40 repeat is required for cytochrome c binding and regulated activation of procaspase-9. J. Biol. Chem., 275, 8461-8468.
39. Acehan, D., Jiang, X., Morgan, D.G., Heuser, J.E., Wang, X. and Akey, C.W. (2002) Three-dimensional structure of the apoptosome: Implications for assembly, procaspase-9 binding, and activation. Mol. Cell, 9, 423-432.
40. Yu, X., Acehan, D., Menetret, J.F., Booth, C.R., Ludtke, S.J., Riedl, S.J., Shi, Y., Wang, X. and Akey, C.W. (2005) A structure of the human apoptosome at 12.8 A resolution provides insights into this cell death platform. Structure (Camb.), 13, 1725-1735.
41. Consortium, T.C.S.a.A. (2005) Initial sequence of the chimpanzee genome and comparison with the human genome. Nature, 437, 69-87.
42. Nielsen, R., Bustamante, C., Clark, A.G., Glanowski, S., Sackton, T.B., Hubisz, M.J., Fledel-Alon, A., Tanenbaum, D.M., Civello, D., White, T.J. et al. (2005) A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol., 3, e170.
43. Eyre-Walker, A., Keightley, P.D., Smith, N.G. and Gaffney, D. (2002) Quantifying the slightly deleterious mutation model of molecular evolution. Mol. Biol. Evol., 19, 2142-2149.
44. Earnshaw, W.C., Martins, L.M. and Kaufmann, S.H. (1999) Mammalian caspases: Structure, activation, substrates, and functions during apoptosis. Annu. Rev. Biochem., 68, 383-424.
45. Janicke, R.U., Ng, P., Sprengart, M.L. and Porter, A.G. (1998) Caspase-3 is required for alpha-fodrin cleavage but dispensable for cleavage of other death substrates in apoptosis. J. Biol. Chem., 273, 15540-15545.
46. Wang, Y. and Gu, X. (2001) Functional divergence in the caspase gene family and altered functional constraints: Statistical analysis and prediction. Genetics, 158, 1311-1320.
47. Li, W.H. (1993) Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J. Mol. Evol., 36, 96-99.
48. Tzeng, Y.H., Pan, R. and Li, W.H. (2004) Comparison of three methods for estimating rates of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol., 21, 2290-2298.
49. Choi, S.S. and Lahn, B.T. (2003) Adaptive evolution of MRG, a neuron-specific gene family implicated in nociception. Genome Res., 13, 2252-2259.