Skip to main content

Advertisement

Log in

Human body temperature and new approaches to constructing temperature-sensitive bacterial vaccines

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Many of the live human and animal vaccines that are currently in use are attenuated by virtue of their temperature-sensitive (TS) replication. These vaccines are able to function because they can take advantage of sites in mammalian bodies that are cooler than the core temperature, where TS vaccines fail to replicate. In this article, we discuss the distribution of temperature in the human body, and relate how the temperature differential can be exploited for designing and using TS vaccines. We also examine how one of the coolest organs of the body, the skin, contains antigen-processing cells that can be targeted to provoke the desired immune response from a TS vaccine. We describe traditional approaches to making TS vaccines, and highlight new information and technologies that are being used to create a new generation of engineered TS vaccines. We pay particular attention to the recently described technology of substituting essential genes from Arctic bacteria for their homologues in mammalian pathogens as a way of creating TS vaccines.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Calmette LCA, Guérin C, Négre L, Bouquet A (1927) Sur la vaccination preventive des enfants nouveau-nes contre la tuberculose par le BCG. Ann Inst Pasteur 41:201–232

    Google Scholar 

  2. Germanier R, Fuer E (1975) Isolation and characterization of Gal E mutant Ty 21a of Salmonella typhi: a candidate strain for a live, oral typhoid vaccine. J Infect Dis 131:553–558

    Article  PubMed  CAS  Google Scholar 

  3. Mariak Z, Lewko J, Luczaj J, Polocki B, White MD (1994) The relationship between directly measured human cerebral and tympanic temperatures during changes in brain temperatures. Eur J Appl Physiol Occup Physiol 69:545–549

    Article  PubMed  CAS  Google Scholar 

  4. Mellergard P, Nordstrom CH (1990) Epidural temperature and possible intracerebral temperature gradients in man. Br J Neurosurg 4:31–38

    Article  PubMed  CAS  Google Scholar 

  5. McFadden ER Jr, Pichurko BM, Bowman HF, Ingenito E, Burns S, Dowling N, Solway J (1985) Thermal mapping of the airways in humans. J Appl Physiol 58:564–570

    Article  PubMed  Google Scholar 

  6. Cabanac M, Massonnet B (1977) Thermoregulatory responses as a function of core temperature in humans. J Physiol (Lond) 265:587–596

    CAS  Google Scholar 

  7. Hammel HT, Jackson DC, Stolwijk JA, Hardy JD, Stromme SB (1963) Temperature regulation by hypothalamic proportional control with an adjustable set point. J Appl Physiol 18:1146–1154

    PubMed  CAS  Google Scholar 

  8. Lopez M, Sessler DI, Walter K et al (1994) Rate- and gender-dependence of the sweating, vasoconstriction, and shivering thresholds in humans. Anesthesiology 80:780–788

    Article  PubMed  CAS  Google Scholar 

  9. Mekjavic IB, Sundberg CJ, Linnarsson D (1991) Core temperature “null zone”. J Appl Physiol 71:1289–1295

    PubMed  CAS  Google Scholar 

  10. Cabanac M (2006) Adjustable set point: to honor Harold T Hammel. J Appl Physiol 100:1338–1346

    Article  PubMed  Google Scholar 

  11. Bligh J (1984) Regulation of body temperature in man and other mammals. In: Shitzer A, Eberhart R (eds) Heat transfer and medicine in biology. Plenum Pub Co, pp 15–51

  12. Wenger CB (2008) Human adaptations to hot environments. In: Taylor N, Groeller H (eds) Physiological bases of human performance during work and exercise. Elsevier, London

  13. Kellogg DL Jr (2006) In vivo mechanisms of cutaneous vasodilation and vasoconstriction in humans during thermoregulatory challenges. J Appl Physiol 100:1709–1718

    Article  PubMed  CAS  Google Scholar 

  14. Stephenson LA, Kolka MA (1988) Effect of gender, circadian period and sleep loss on thermal responses during exercise. In: Pandolf KB, Sawka MN, Gonzalez RR (eds) Human performance physiology and environmental medicine at terrestrial extremes. Benchmark Inc, Indianapolis, pp 267–304

    Google Scholar 

  15. Krauchi K, Wirz-Justice A (1994) Circadian rhythm of heat production, heart rate, and skin and core temperature under unmasking conditions in men. Am J Physiol 267:R819–R829

    PubMed  CAS  Google Scholar 

  16. Marsh SA, Jenkins DG (2002) Physiological responses to the menstrual cycle: implications for the development of heat illness in female athletes. Sports Med 32:601–614

    Article  PubMed  Google Scholar 

  17. Young A (1988) Human adaptation to cold. In: Pandolf KB, Sawka MN, Gonzalez RR (eds) Human performance physiology and environmental medicine at terrestrial extremes. Benchmark Inc, Indianapolis, pp 401–434

    Google Scholar 

  18. LeBlanc J (1975) Man in the cold Charles C Thomas. Springfield, Illinois

  19. Cheshire WP, Freeman R (2003) Disorders of sweating. Semin Neurol 23:399–406. doi:10.1055/s-2004-817724

    Article  PubMed  Google Scholar 

  20. Banchereau J, Steinman RM (1998) Dendritic cells and the control of immunity. Nature 392:245–252

    Article  PubMed  CAS  Google Scholar 

  21. Sallusto F, Schaerli P, Loetscher P, Schaniel C, Lenig D, Mackay CR, Qin S, Lanzavecchia A (1998) Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation. Eur J Immunol 28:2760–2769

    Article  PubMed  CAS  Google Scholar 

  22. Henri S, Vremec D, Kamath A, Waithman J, Williams S, Benoist C, Burnham K, Saeland S, Handman E, Shortman K (2001) The dendritic cell populations of mouse lymph nodes. J Immunol 167:741–748

    PubMed  CAS  Google Scholar 

  23. Ginhoux F, Collin MP, Bogunovic M, Abel M, Leboeuf M, Helft J, Ochando J, Kissenpfennig A, Malissen B, Grisotto M, Snoeck H, Randolph G, Merad M (2007) Blood-derived dermal langerin + dendritic cells survey the skin in the steady state. J Exp Med 204:3133–3146

    Article  PubMed  CAS  Google Scholar 

  24. Bedoui S, Whitney PG, Waithman J, Eidsmo L, Wakim L, Caminschi I, Allan RS, Wojtasiak M, Shortman K, Carbone FR, Brooks AG, Heath WR (2009) Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat Immunol 10:488–495

    Article  PubMed  CAS  Google Scholar 

  25. Sen D, Forrest L, Kepler TB, Parker I, Cahalan MD (2010) Selective and site-specific mobilization of dermal dendritic cells and Langerhans cells by Th1- and Th2-polarizing adjuvants. Proc Natl Acad Sci USA 107:8334–8339

    Article  PubMed  CAS  Google Scholar 

  26. Allen WP (1962) Immunity against tularemia: passive protection of mice by transfer of immune tissues. J Exp Med 115:411–420

    Article  PubMed  CAS  Google Scholar 

  27. North RJ (1973) Importance of thymus-derived lymphocytes in cell-mediated immunity to infection. Cell Immunol 7:166–176

    Article  PubMed  CAS  Google Scholar 

  28. Orme IM, Collins FM (1983) Protection against Mycobacterium tuberculosis infection by adoptive immunotherapy. Requirement for T cell-deficient recipients. J Exp Med 158:74–83

    Article  PubMed  CAS  Google Scholar 

  29. Gelb J Jr, King DJ, Wisner WA, Ruggeri PA (1996) Attenuation of lentogenic Newcastle disease virus strain B-1 by cold adaptation. Avian Dis 40:605–612

    Article  PubMed  Google Scholar 

  30. Maassab HF, DeBorde DC (1985) Development and characterization of cold-adapted viruses for use as live virus vaccines. Vaccine 3:355–369

    Article  PubMed  CAS  Google Scholar 

  31. Matsuno S, Murakami S, Takagi M, Hayashi M, Inouye S, Hasegawa A, Fukai K (1987) Cold-adaptation of human rotavirus. Virus Res 7:273–280

    Article  PubMed  CAS  Google Scholar 

  32. Chapin M, Dubes GR (1956) Cold-adapted genetic variants of polio viruses. Science 124:586–587

    PubMed  CAS  Google Scholar 

  33. Plotkin SA, Farquhar JD, Katz M, Buser F (1969) Attenuation of RA 27–3 rubella virus in WI-38 human diploid cells. Am J Dis Child 118:178–185

    PubMed  CAS  Google Scholar 

  34. Skiadopoulos MH, Durbin AP, Tatem JM, Wu SL, Paschalis M, Tao T, Collins PL, Murphy BR (1998) Three amino acid substitutions in the L protein of the human parainfluenza virus type 3 cp45 live attenuated vaccine candidate contribute to its temperature-sensitive and attenuation phenotypes. J Virol 72:1762–1768

    PubMed  CAS  Google Scholar 

  35. Skiadopoulos MH, Surman S, Tatem JM, Paschalis M, Wu SL, Udem SA, Durbin AP, Collins PL, Murphy BR (1999) Identification of mutations contributing to the temperature-sensitive, cold-adapted, and attenuation phenotypes of the live-attenuated cold-passage 45 (cp45) human parainfluenza virus 3 candidate vaccine. J Virol 73:1374–1381

    PubMed  CAS  Google Scholar 

  36. Subbarao EK, Park EJ, Lawson CM, Chen AY, Murphy BR (1995) Sequential addition of temperature-sensitive missense mutations into the PB2 gene of influenza A transfectant viruses can effect an increase in temperature sensitivity and attenuation and permits the rational design of a genetically engineered live influenza A virus vaccine. J Virol 69:5969–5977

    PubMed  CAS  Google Scholar 

  37. Maassab HF (1967) Adaptation and growth characteristics of influenza virus at 25 degrees c. Nature 213:612–614

    Article  PubMed  CAS  Google Scholar 

  38. Jin H, Lu B, Zhou H, Ma C, Zhao J, Yang CF, Kemble G, Greenberg H (2003) Multiple amino acid residues confer temperature sensitivity to human influenza virus vaccine strains (FluMist) derived from cold-adapted A/Ann Arbor/6/60. Virology 306:18–24

    Article  PubMed  CAS  Google Scholar 

  39. Jin H, Zhou H, Lu B, Kemble G (2004) Imparting temperature sensitivity and attenuation in ferrets to A/Puerto Rico/8/34 influenza virus by transferring the genetic signature for temperature sensitivity from cold-adapted A/Ann Arbor/6/60. J Virol 78:995–998

    Article  PubMed  CAS  Google Scholar 

  40. Chan W, Zhou H, Kemble G, Jin H (2008) The cold-adapted and temperature-sensitive influenza A/Ann Arbor/6/60 virus, the master donor virus for live attenuated influenza vaccines, has multiple defects in replication at the restrictive temperature. Virology 380:304–311

    Article  PubMed  CAS  Google Scholar 

  41. Belshe RB, Edwards KM, Vesikari T, Black SV, Walker RE, Hultquist M, Kemble G, Connor EM (2007) Live attenuated versus inactivated influenza vaccine in infants and young children. N Engl J Med 356:685–696

    Article  PubMed  CAS  Google Scholar 

  42. King JC Jr, Treanor J, Fast PE, Wolff M, Yan L, Iacuzio D, Readmond B, O’Brien D, Mallon K, Highsmith WE, Lambert JS, Belshe RB (2000) Comparison of the safety, vaccine virus shedding, and immunogenicity of influenza virus vaccine, trivalent, types A and B, live cold-adapted, administered to human immunodeficiency virus (HIV)-infected and non-HIV-infected adults. J Infect Dis 181:725–728

    Article  PubMed  Google Scholar 

  43. Chalmers WS, Simpson J, Lee SJ, Baxendale W (1997) Use of a live chlamydial vaccine to prevent ovine enzootic abortion. Vet Rec 141:63–67

    Article  PubMed  CAS  Google Scholar 

  44. Rodolakis A (1983) In vitro and in vivo properties of chemically induced temperature-sensitive mutants of Chlamydia psittaci var. ovis: screening in a murine model. Infect Immun 42:525–530

    PubMed  CAS  Google Scholar 

  45. Rodolakis A, Souriau A (1983) Response of ewes to temperature-sensitive mutants of Chlamydia psittaci (var ovis) obtained by NTG mutagenesis. Ann Rech Vet 14:155–161

    PubMed  CAS  Google Scholar 

  46. Markham JF, Morrow CJ, Scott PC, Whithear KG (1998) Safety of a temperature-sensitive clone of Mycoplasma synoviae as a live vaccine. Avian Dis 42:677–681

    Article  PubMed  CAS  Google Scholar 

  47. Markham JF, Morrow CJ, Whithear KG (1998) Efficacy of a temperature-sensitive Mycoplasma synoviae live vaccine. Avian Dis 42:671–676

    Article  PubMed  CAS  Google Scholar 

  48. Morrow CJ, Markham JF, Whithear KG (1998) Production of temperature-sensitive clones of Mycoplasma synoviae for evaluation as live vaccines. Avian Dis 42:667–670

    Article  PubMed  CAS  Google Scholar 

  49. Barbour EK, Hamadeh SK, Eidt A (2000) Infection and immunity in broiler chicken breeders vaccinated with a temperature-sensitive mutant of Mycoplasma gallisepticum and impact on performance of offspring. Poult Sci 79:1730–1735

    PubMed  CAS  Google Scholar 

  50. Jackwood MW, Saif YM (1985) Efficacy of a commercial turkey coryza vaccine (Art-Vax) in turkey poults. Avian Dis 29:1130–1139

    Article  PubMed  CAS  Google Scholar 

  51. Akerley BJ, Rubin EJ, Novick VL, Amaya K, Judson N, Mekalanos JJ (2002) A genome-scale analysis for identification of genes required for growth or survival of Haemophilus influenzae. Proc Natl Acad Sci USA 99:966–971

    Article  PubMed  CAS  Google Scholar 

  52. de Berardinis V, Vallenet D, Castelli V, Besnard M, Pinet A, Cruaud C, Samair S, Lechaplais C, Gyapay G, Richez C, Durot M, Kreimeyer A, Le Fevre F, Schachter V, Pezo V, Doring V, Scarpelli C, Medigue C, Cohen GN, Marliere P, Salanoubat M, Weissenbach J (2008) A complete collection of single-gene deletion mutants of Acinetobacter baylyi ADP1. Mol Syst Biol 4:174

    PubMed  Google Scholar 

  53. Forsyth RA, Haselbeck RJ, Ohlsen KL, Yamamoto RT, Xu H, Trawick JD, Wall D, Wang L, Brown-Driver V, Froelich JM, KG C, King P, McCarthy M, Malone C, Misiner B, Robbins D, Tan Z, Zhu Zy ZY, Carr G, Mosca DA, Zamudio C, Foulkes JG, Zyskind JW (2002) A genome-wide strategy for the identification of essential genes in Staphylococcus aureus. Mol Microbiol 43:1387–1400

    Article  PubMed  CAS  Google Scholar 

  54. Gallagher LA, Ramage E, Jacobs MA, Kaul R, Brittnacher M, Manoil C (2007) A comprehensive transposon mutant library of Francisella novicida, a bioweapon surrogate. Proc Natl Acad Sci USA 104:1009–1014

    Article  PubMed  CAS  Google Scholar 

  55. Gerdes SY, Scholle MD, Campbell JW, Balazsi G, Ravasz E, Daugherty MD, Somera AL, Kyrpides NC, Anderson I, Gelfand MS, Bhattacharya A, Kapatral V, D’Souza M, Baev MV, Mseeh F, Fonstein MY, Overbeek R, Barabasi A-L, Oltvai ZN, Osterman AL (2003) Experimental determination and system level analysis of essential genes in Escherichia coli MG1655. J Bacteriol 185:5673–5684

    Article  PubMed  CAS  Google Scholar 

  56. Glass JI, Assad-Garcia N, Alperovich N, Yooseph S, Lewis MR, Maruf M, Hutchison CA 3rd, Smith HO, Venter JC (2006) Essential genes of a minimal bacterium. Proc Natl Acad Sci USA 103:425–430

    Article  PubMed  CAS  Google Scholar 

  57. Jacobs MA, Alwood A, Thaipisuttikul I, Spencer D, Haugen E, Ernst S, Will O, Kaul R, Raymond C, Levy R, Chun-Rong L, Guenthner D, Bovee D, Olson MV, Manoil C (2003) Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 100:14339–14344

    Article  PubMed  CAS  Google Scholar 

  58. Ji Y, Zhang B, Van SF, Horn Warren P, Woodnutt G, Burnham MK, Rosenberg M (2001) Identification of critical staphylococcal genes using conditional phenotypes generated by antisense RNA. Science 293:2266–2269

    Article  PubMed  CAS  Google Scholar 

  59. Knuth K, Niesalla H, Hueck CJ, Fuchs TM (2004) Large-scale identification of essential Salmonella genes by trapping lethal insertions. Mol Microbiol 51:1729–1744

    Article  PubMed  CAS  Google Scholar 

  60. Kobayashi K, Ehrlich SD, Albertini A, Amati G, Andersen KK, Arnaud M, Asai K, Ashikaga S, Aymerich S, Bessieres P, Boland F, Brignell SC, Bron S, Bunai K, Chapuis J, Christiansen LC, Danchin A, Debarbouille M, Dervyn E, Deuerling E, Devine K, Devine SK, Dreesen O, Errington J, Fillinger S, Foster SJ, Fujita Y, Galizzi A, Gardan R, Eschevins C, Fukushima T, Haga K, Harwood CR, Hecker M, Hosoya D, Hullo MF, Kakeshita H, Karamata D, Kasahara Y, Kawamura F, Koga K, Koski P, Kuwana R, Imamura D, Ishimaru M, Ishikawa S, Ishio I, Le Coq D, Masson A, Mauel C, Meima R, Mellado RP, Moir A, Moriya S, Nagakawa E, Nanamiya H, Nakai S, Nygaard P, Ogura M, Ohanan T, O’Reilly M, O’Rourke M, Pragai Z, Pooley HM, Rapoport G, Rawlins JP, Rivas LA, Rivolta C, Sadaie A, Sadaie Y, Sarvas M, Sato T, Saxild HH, Scanlan E, Schumann W, Seegers JF, Sekiguchi J, Sekowska A, Seror SJ, Simon M, Stragier P, Studer R, Takamatsu H, Tanaka T, Takeuchi M, Thomaides HB, Vagner V, van Dijl JM, Watabe K, Wipat A, Yamamoto H, Yamamoto M, Yamamoto Y, Yamane K, Yata K, Yoshida K, Yoshikawa H, Zuber U, Ogasawara N (2003) Essential Bacillus subtilis genes. Proc Natl Acad Sci USA 100:4678–4683

    Article  PubMed  CAS  Google Scholar 

  61. Salama NR, Shepherd B, Falkow S (2004) Global transposon mutagenesis and essential gene analysis of Helicobacter pylori. J Bacteriol 186:7926–7935

    Article  PubMed  CAS  Google Scholar 

  62. Sassetti CM, Boyd DH, Rubin EJ (2003) Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48:77–84

    Article  PubMed  CAS  Google Scholar 

  63. Thanassi JA, Hartman-Neumann SL, Dougherty TJ, Dougherty BA, Pucci MJ (2002) Identification of 113 conserved essential genes using a high-throughput gene disruption system in Streptococcus pneumoniae. Nucleic Acids Res 30:3152–3162

    Article  PubMed  CAS  Google Scholar 

  64. Xu HH, Trawick JD, Haselbeck RJ, Forsyth RA, Yamamoto RT, Archer R, Patterson J, Allen M, Froelich JM, Taylor I, Nakaji D, Maile R, Kedar GC, Pilcher M, Brown-Driver V, McCarthy M, Files A, Robbins D, King P, Sillaots S, Malone C, Zamudio CS, Roemer T, Wang L, Youngman PJ, Wall D (2010) Staphylococcus aureus TargetArray: comprehensive differential essential gene expression as a mechanistic tool to profile antibacterials. Antimicrob Agents Chemother 54:3659–3670

    Article  PubMed  CAS  Google Scholar 

  65. Duplantis BN, Osusky M, Schmerk CL, Ross DR, Bosio CM, Nano FE (2010) Essential genes from Arctic bacteria used to construct stable, temperature-sensitive bacterial vaccines. Proc Natl Acad Sci USA 107:13456–13460

    Article  PubMed  CAS  Google Scholar 

  66. de Lorenzo V (2010) Genes that move the window of viability of life: Lessons from bacteria thriving at the cold extreme: mesophiles can be turned into extremophiles by substituting essential genes. Bioessays 33:38–42

    Article  Google Scholar 

  67. Duplantis BN, Bosio CM, Nano FE (2011) Temperature-sensitive bacterial pathogens generated by the substitution of essential genes from cold-loving bacteria: potential use as live vaccines. J Mol Med. doi:10.1007/s00109-010-0721-3

  68. Aurilia V, Parracino A, Saviano M, Rossi M, D’Auria S (2007) The psychrophilic bacterium Pseudoalteromonas halosplanktis TAC125 possesses a gene coding for a cold-adapted feruloyl esterase activity that shares homology with esterase enzymes from gamma-proteobacteria and yeast. Gene 397:51–57

    Article  PubMed  CAS  Google Scholar 

  69. Medigue C, Krin E, Pascal G, Barbe V, Bernsel A, Bertin PN, Cheung F, Cruveiller S, D’Amico S, Duilio A, Fang G, Feller G, Ho C, Mangenot S, Marino G, Nilsson J, Parrilli E, Rocha EP, Rouy Z, Sekowska A, Tutino ML, Vallenet D, von Heijne G, Danchin A (2005) Coping with cold: the genome of the versatile marine Antarctica bacterium Pseudoalteromonas haloplanktis TAC125. Genome Res 15:1325–1335

    Article  PubMed  CAS  Google Scholar 

  70. Methe BA, Karen E, Nelson KE, Deming JW, Momen B, Melamud E, Xijun Zhang X, John Moult J, Madupu R, Nelson WC, Dodson RJ, Brinkac LM, Daugherty SC, Durkin AS, DeBoy RT, Kolonay JF, Sullivan SA, Zhou L, Davidsen TM, Wu M, Huston AL, Lewis M, Weaver B, Weidman JW, Khouri H, Utterback TR, Feldblyum TV, Fraser CM (2005) The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses. Proceedings of the National Academy of Sciences 102:10913–10918

    Article  CAS  Google Scholar 

  71. Rohmer L, Fong C, Abmayr S, Wasnick M, Larson Freeman TJ, Radey M, Guina T, Svensson K, Hayden HS, Jacobs M, Gallagher LA, Manoil C, Ernst RK, Drees B, Buckley D, Haugen E, Bovee D, Zhou Y, Chang J, Levy R, Lim R, Gillett W, Guenthener D, Kang A, Shaffer SA, Taylor G, Chen J, Gallis B, D’Argenio DA, Forsman M, Olson MV, Goodlett DR, Kaul R, Miller SI, Brittnacher MJ (2007) Comparison of Francisella tularensis genomes reveals evolutionary events associated with the emergence of human pathogenic strains. Genome Biol 8:R102

    Article  PubMed  Google Scholar 

  72. Sharma J, Li Q, Mishra BB, Georges MJ, Teale JM (2009) Vaccination with an attenuated strain of Francisella novicida prevents T-cell depletion and protects mice infected with the wild-type strain from severe sepsis. Infect Immun 77:4314–4326

    Article  PubMed  CAS  Google Scholar 

  73. Anthony LS, Gu MZ, Cowley SC, Leung WW, Nano FE (1991) Transformation and allelic replacement in Francisella spp. J Gen Microbiol 137:2697–2703

    PubMed  CAS  Google Scholar 

  74. Salis HM, Mirsky EA, Voigt CA (2009) Automated design of synthetic ribosome binding sites to control protein expression. Nat Biotechnol 27:946–950

    Article  PubMed  CAS  Google Scholar 

  75. Grosjean H, Fiers W (1982) Preferential codon usage in prokaryotic genes: the optimal codon-anticodon interaction energy and the selective codon usage in efficiently expressed genes. Gene 18:199–209

    Article  PubMed  CAS  Google Scholar 

  76. Rocha EP (2004) Codon usage bias from tRNA’s point of view: redundancy, specialization, and efficient decoding for translation optimization. Genome Res 14:2279–2286

    Article  PubMed  CAS  Google Scholar 

  77. Gutman GA, Hatfield GW (1989) Nonrandom utilization of codon pairs in Escherichia coli. Proc Natl Acad Sci USA 86:3699–3703

    Article  PubMed  CAS  Google Scholar 

  78. Meng Q, Switzer RL (2001) Regulation of transcription of the Bacillus subtilis pyrG gene, encoding cytidine triphosphate synthetase. J Bacteriol 183:5513–5522

    Article  PubMed  CAS  Google Scholar 

  79. Meng Q, Switzer RL (2002) cis-acting sequences of Bacillus subtilis pyrG mRNA essential for regulation by antitermination. J Bacteriol 184:6734–6738

    Article  PubMed  CAS  Google Scholar 

  80. Meng Q, Turnbough CL Jr, Switzer RL (2004) Attenuation control of pyrG expression in Bacillus subtilis is mediated by CTP-sensitive reiterative transcription. Proc Natl Acad Sci USA 101:10943–10948

    Article  PubMed  Google Scholar 

  81. Voigt CA (2006) Genetic parts to program bacteria. Curr Opin Biotechnol 17:548–557

    Article  PubMed  CAS  Google Scholar 

  82. Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S, Wu D, Eisen JA, Hoffman JM, Remington K, Beeson K, Tran B, Smith H, Baden-Tillson H, Stewart C, Thorpe J, Freeman J, Andrews-Pfannkoch C, Venter JE, Li K, Kravitz S, Heidelberg JF, Utterback T, Rogers YH, Falcon LI, Souza V, Bonilla-Rosso G, Eguiarte LE, Karl DM, Sathyendranath S, Platt T, Bermingham E, Gallardo V, Tamayo-Castillo G, Ferrari MR, Strausberg RL, Nealson K, Friedman R, Frazier M, Venter JC (2007) The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol 5:e77

    Article  PubMed  Google Scholar 

  83. Coleman JR, Papamichail D, Skiena S, Futcher B, Wimmer E, Mueller S (2008) Virus attenuation by genome-scale changes in codon pair bias. Science 320:1784–1787

    Article  PubMed  CAS  Google Scholar 

  84. Mueller S, Coleman JR, Papamichail D, Ward CB, Nimnual A, Futcher B, Skiena S, Wimmer E (2010) Live attenuated influenza virus vaccines by computer-aided rational design. Nat Biotechnol 28:723–726

    Article  PubMed  CAS  Google Scholar 

  85. Mueller S, Papamichail D, Coleman JR, Skiena S, Wimmer E (2006) Reduction of the rate of poliovirus protein synthesis through large-scale codon deoptimization causes attenuation of viral virulence by lowering specific infectivity. J Virol 80:9687–9696

    Article  PubMed  CAS  Google Scholar 

  86. Posfai G, Plunkett G 3rd, Feher T, Frisch D, Keil GM, Umenhoffer K, Kolisnychenko V, Stahl B, Sharma SS, de Arruda M, Burland V, Harcum SW, Blattner FR (2006) Emergent properties of reduced-genome Escherichia coli. Science 312:1044–1046

    Article  PubMed  CAS  Google Scholar 

  87. Gibson DG, Glass JI, Lartigue C, Noskov VN, Chuang RY, Algire MA, Benders GA, Montague MG, Ma L, Moodie MM, Merryman C, Vashee S, Krishnakumar R, Assad-Garcia N, Andrews-Pfannkoch C, Denisova EA, Young L, Qi ZQ, Segall-Shapiro TH, Calvey CH, Parmar PP, Hutchison CA 3rd, Smith HO, Venter JC (2010) Creation of a bacterial cell controlled by a chemically synthesized genome. Science 329:52–56

    Article  PubMed  CAS  Google Scholar 

  88. Lartigue C, Vashee S, Algire MA, Chuang RY, Benders GA, Ma L, Noskov VN, Denisova EA, Gibson DG, Assad-Garcia N, Alperovich N, Thomas DW, Merryman C, Hutchison CA III, Smith HO, Venter JC, Glass JI (2009) Creating bacterial strains from genomes that have been cloned and engineered in yeast. Science 325:1693–1696

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Jordon Drew for artwork and Sheila Potter for editorial assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Francis E. Nano.

Rights and permissions

Reprints and permissions

About this article

Cite this article

White, M.D., Bosio, C.M., Duplantis, B.N. et al. Human body temperature and new approaches to constructing temperature-sensitive bacterial vaccines. Cell. Mol. Life Sci. 68, 3019–3031 (2011). https://doi.org/10.1007/s00018-011-0734-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-011-0734-2

Keywords

Navigation