Seasonal and Physiological Variations of Phlebotomus papatasi Salivary Gland Antigens in Central Iran

  • Nasibeh Hosseini-Vasoukolaei Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran.
  • AhmadReza Mahmoudi Monoclonal Antibody Research Center, Avicenna Research Institute, ACECR, Tehran, Iran.
  • Ali Khamesipour Center for Research and Training in Skin Diseases and Leprosy, Tehran University of Medical Sciences, Tehran, Iran.
  • MohammadReza Yaghoobi-Ershadi Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran.
  • Shaden Kamhawi Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institute of Health, Rockville, USA.
  • Jesus G Valenzuela Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institute of Health, Rockville, USA.
  • MohammadHossein Arandian Esfahan Health Research Station, National Institute of Health Research, Tehran University of Medical SciencesEsfahan, Iran.
  • Hossein Mirhendi Department of Medical Parasitology and Mycology, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran.
  • Shaghayegh Emami Monoclonal Antibody Research Center, Avicenna Research Institute, ACECR, Tehran, Iran.
  • Zahra Saeidi Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran.
  • Farah Idali Reproductive Immunology Research Center, Avicenna Research Institute, ACECR, Tehran, Iran.
  • Reza Jafari Esfahan Health Research Station, National Institute of Health Research, Tehran University of Medical SciencesEsfahan, Iran.
  • Mahmood Jeddi-Tehrani Monoclonal Antibody Research Center, Avicenna Research Institute, ACECR, Tehran, Iran.
  • AmirAhmad Akhavan Mail Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran.
Keywords:
Antibody response, Phlebotomus papatasi, Rhombomys opimus, Salivary gland antigens, Iran

Abstract

Background: Sand fly saliva helps parasite establishment and induce immune responses in vertebrate hosts. In the current study, we investigated the modulation of Phlebotomus papatasi salivary gland antigen expression by sea­sonal and biological factors.Methods: Sand flies were grouped according to physiological stages such as unfed, fed, semi-gravid, gravid, parous, nulliparous, infected or non-infected with Leishmania major and based on the season in which they were collected. Salivary gland antigens (SGAs) were analyzed using SDS-PAGE and the antibody response against SGAs in Rhombomys opimus was determined by ELISA and Western blot.Results: The highest protein content was found in the salivary glands of unfed sand flies. The saliva content was higher in parous compared to nulliparous, in summer compared to spring, and in Leishmania-infected compared to non-infected flies. The salivary gland lysate (SGL) electrophoretic pattern variations were observed among sand flies with various physiological stages particularly from 4–9 protein bands of 14–70 kDa. The SGL of unfed and gravid flies had extra protein bands compared to fed and semi-gravid sand flies. There was missing protein bands in SGL of parous compared to nulliparous; and in summer compared to spring collected flies. Rhombomys opimus se­rum reacted strongly with an antigenic band of around 28 kDa in the SGL of all sand fly groups.Conclusion: Certain biological and environmental characteristics of wild populations of vector sand flies affect the protein content and antigenicity of saliva. This might have an important implication in the design of vector-based vaccines.

Author Biography

Reza Jafari, Esfahan Health Research Station, National Institute of Health Research, Tehran University of Medical SciencesEsfahan, Iran.

References

Akhavan AA, Mirhendi H, Khamesipour A, Alimohammadian MH, Rassi Y, Bates P, Kamhawi S, Valenzuela JG, Arandian MH, Abdoli H, Jalali-zand N, Jafari R, Shareghi N, Ghanei M, Yaghoobi- Ershadi MR (2010a) Leishmania spe- cies: detection and identification by nested PCR assay from skin samples of rodent reservoirs. Exp Parasitol.126: 552–556.

Akhavan AA, Yaghoobi-Ershadi MR, Khame- sipour A, Miarhendi H, Alimohammadian MH, Rassi Y, Arandian MH, Jafari R, Abdoli H, Shareghi N, Ghanei M, Jalali- zand N (2010b) Dynamics of Leishmania infection rates in Rhombomys opimus (Rodentia: Gerbillinae) population of an endemic focus of zoonotic cutane- ous leishmaniasis in Iran. Bull Soc Pathol Exot.103: 84–89.

Akhavan AA (2011) Immune response of great gerbil against Phlebotomus papatasi saliva: Immune response of Rhombomys opimus against Phlebotomus papatasi saliva and its role in Leishmania major infection. Lambert Academic Publish- ing, Germany.

Akhavan AA, Ghods R, Jeddi-Tehrani M, Yaghoobi-Ershadi MR, Khamesipour A, Mahmoudi AR (2011) Production and purification of anti-Rhombomys opimus immunoglobulins. Iran J Ar- thropod Borne Dis. 5: 69–76.

Belkaid Y, Kamhawi S, Modi G, Valenzuela JG, Noben-Trauth N, Rowton E, Ribeiro JM, Sacks DL (1998) Development of a natural model of cutaneous leish- maniasis: powerful effects of vector saliva and saliva pre-exposure on the long-term outcome of Leishmania major infection in the mouse ear dermis. J Exp Med.188: 1941–1953.

Belkaid Y, Valenzuela JG, Kamhawi S, Rowton E, Sacks DL, Ribeiro JM (2000) De- layed-type hypersensitivity to Phlebo- tomus papatasi sand fly bite: an adap- tive response induced by the fly? Proc Natl Acad Sci USA.97: 6704–6709.

Ben Hadj Ahmed S, Chelbi I, Kaabi B, Cherni S, Derbali M, Zhioua E (2010) Differences in the salivary effects of wild-caught versus colonized Phlebo- tomus papatasi (Diptera: Psychodidae) on the development of zoonotic cu- taneous leishmaniasis in BALB/c mice. J Med Entomol.47: 74–79.

Cerna P, Mikes L, Volf P (2002) Salivary gland hyaluronidase in various species of phlebotomine sand flies (Diptera: psychodidae). Insect Biochem Mol Biol.32: 1691–1697.

Coutinho-Abreu IV, Mukbel R, Hanafi HA, Fawaz EY, El-Hossary SS, Wadsworth M, Stayback G, Pitts DA, Abo- Shehada M, Hoel DF, Kamhawi S, Ramalho- Ortigao M, McDowell MA (2011) Expression plasticity of Phlebotomus papatasi salivary gland genes in dis- tinct ecotopes through the sand fly season. BMC Ecol. 11: 24.

Gomes R, Oliveira F, Teixeira C, Meneses C, Gilmore DC, Elnaiem DE, Kamhawi S, Valenzuela JG (2012) Immunity to sand fly salivary protein LJM11 modu- lates host response to vector-transmit- ted leishmania conferring ulcer-free pro- tection. J Invest Dermatol. 132: 2735–2743.

Hamarsheh O, Presber W, Yaghoobi-Ershadi MR, Amro A, Al-Jawabreh A, Sawalha S (2009) Population structure and geo- graphical subdivision of the Leishmania major vector Phlebotomus papatasi as revealed by microsatellite variation. Med Vet Entomol.23: 69–77.

Heukeshoven J, Dernick R (1985) Simpli- fied method for silver staining of pro- teins in polyacrylamide gels and the mechanism of silver staining. Electro- phoresis. 6: 103–112.

Kamhawi S, Belkaid Y, Modi G, Rowton E, Sacks DL (2000) Protection against cutaneous leishmaniasis resulting from bites of uninfected sand flies. Science.290: 1351–1354.

Kamhawi S (2006) Phlebotomine sand flies and Leishmania parasites: friends or foes? Trends Parasitol. 22: 439–445.

Killick-Kendrick M, Killick-Kendrick R (1991) The initial establishment of sand fly colonies. Parasitologia. 33: 315–320.

Marzouki S, Abdeladhim M, Ben Abdessalem C, Oliveira F, Ferjani B, Gilmore D, Louzir H, Valenzuela JG, Ben Ahmed M (2012) Salivary antigen SP32 is the immunodominant target of the anti- body response to Phlebotomus papatasi bites in humans. PLoS Negl Trop Dis.6(11): e1911.

Modi GB, Tesh RB (1983) A simple tech- nique for mass rearing Lutzomyia longipalpis and Phlebotomus papatasi (Diptera, Psychodidae) in the labora- tory. J Med Entomol. 20: 568–569.

Oliveira F, Lawyer PG, Kamhawi S, Valenzuela JG (2008) Immunity to dis- tinct sand fly salivary proteins primes the anti-Leishmania immune response towards protection or exacerbation of disease. PLoS Negl Trop Dis. 2(4): e226.

Oliveira F, de Carvalho AM, de Oliveira CI (2013) Sand fly saliva-Leishmania-man: the trigger trio. Front Immunol. 4: 375.

Ribeiro JM (1987) Role of saliva in blood- feeding by arthropods. Annu Rev En- tomol. 32: 463–478.

Rohousova I, Ozensoy S, Ozbel Y, Volf P (2005) Detection of species-specific antibody response of human and mice bitten by sand flies. Parasitol.130:493–499.

Seyedi-Rashti MA, Nadim A (1992) The ge- nus Phlebotomus (Diptera: Psychodidae: Phlebotominae) of the countries of the Eastern Mediterranean Region. Iran J Public Health.21: 11–50.

Valenzuela JG, Belkaid Y, Garfiela MK, Mendez S, Kamhawi S, Rowton E, Sacks DL, Ribeiro JM (2001) Toward a defined anti-Leishmania vaccine tar- geting vector antigens: characteriza- tion of a protective salivary protein. J Exp Med. 194: 331–342.

Volf P, Tesarova P, Nohynkova E (2000) Salivary proteins and glycoproteins in sand flies of various species, sex, and age. Med Vet Entomol. 14: 251–256.

Volf P, Rohousova I (2001) Species-specific antigens in salivary glands of phlebo- tomine sand flies. Parasitol.1222: 37–41.

Yaghoobi-Ershadi MR, Javadian E, Tahvildare- Bidruni GH (1995) Leishmania major MON-26 isolated from naturally in- fected Phlebotomus papatasi (Diptera: Psychodidae) in Isfahan Province, Iran. Acta Trop. 59: 279–282.

Yaghoobi-Ershadi MR, Javadian E (1996) Epidemiological study of reservoir hosts in an endemic area of zoonotic cutaneous leishmaniasis in Iran. Bull World Health Organ. 74: 587–590.

Yaghoobi-Ershadi MR, Javadian E (1997) Studies on sandflies in a hyperendemic area of zoonotic cutaneous leishmaniasis in Iran. Indian J Med Res. 105: 61–66.

Yaghoobi-Ershadi MR, Akhavan AA (1999) Entomological survey of sandflies (Dip- tera: Psychodidae) in a new focus of zoonotic cutaneous leishmaniasis in Iran. Acta Trop. 73: 321–326.

Yaghoobi-Ershadi MR, Hanafi-Bojd AA, Akhavan AA, Zahrai-Ramazani AR, Mohebali M (2001) Epidemiological study in a new focus of cutaneous leish- maniasis due to Leishmania major in Ardestan town, central Iran. Acta Trop.79: 115–121.

Yaghoobi-Ershadi MR, Akhavan AA, Zahraei- Ramazani AR, Abai MR, Ebrahimi B, Vafaei-Nezhad R, Hanafi-Bojd AA, Jafari R (2003) Epidemiological study in a new focus of cutaneous leish- maniasis in the Islamic Republic of Iran. East Mediterr Health J.9: 816–826.

Yaghoobi-Ershadi MR, Hakimiparizi M, Zahraei-Ramazani AR, Abdoli H, Akhavan AA, Aghasi M, Arandian MH, Ranjbar AA (2010) Sand fly surveil- lance within an emerging epidemic fo- cus of cutaneous leishmaniasis in south- eastern Iran. Iran J Arthropod Borne Dis. 4: 17–23.

Yaghoobi-Ershadi MR (2012) Phlebotomine sand flies (Diptera: Psychodidae) in Iran and their Role on Leishmania trans- mission. J Arthropod Borne Dis. 6: 1–17.

Published
2016-02-06
How to Cite
1.
Hosseini-Vasoukolaei N, Mahmoudi A, Khamesipour A, Yaghoobi-Ershadi M, Kamhawi S, Valenzuela J, Arandian M, Mirhendi H, Emami S, Saeidi Z, Idali F, Jafari R, Jeddi-Tehrani M, Akhavan A. Seasonal and Physiological Variations of Phlebotomus papatasi Salivary Gland Antigens in Central Iran. J Arthropod Borne Dis. 10(1):39–49.
Section
Original Article