Tuberculosis (TB) is still an important world

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1 Human Leukocyte Antigen-Associated Susceptibility to Pulmonary Tuberculosis* Molecular Analysis of Class II Alleles by DNA Amplification and Oligonucleotide Hybridization in Mexican Patients David Terán-Escandón, MD; Luis Terán-Ortiz, MD; Angel Camarena-Olvera, MSc; Georgina González-Avila, MD; Miguel Angel Vaca-Marín, PhD; Julio Granados, MD; and Moisés Selman, MD, FCCP Background: Pulmonary tuberculosis (PTB) develops by a complex combination of environmental factors with genetic susceptibility. In this context, an association between human leukocyte antigens (HLAs) and tuberculosis has been examined in several populations, but results have been controversial. Design and measurements: A prospective evaluation of class II HLA genotypes was completed by the polymerase chain reaction (PCR) sequence-specific primer technique and PCR sequencespecific oligonucleotide hybridization in a Mexican population. Setting: This study was conducted at the Clinical Service of Tuberculosis and the Department of Immunology, National Institute of Respiratory Diseases, México City, México. Patients: Four groups were examined: 95 healthy subjects; 50 nonimmunosuppressed PTB patients; 15 HIV-infected patients (stage IVc in the Centers for Disease Control and Prevention [CDC] classification system for AIDS) with PTB; and 37 HIV-infected patients in the asymptomatic stage (CDC stage II). Results: The frequencies of alleles DQA1*0101 (odds ratio [OR], 6.18; 95% confidence interval [CI], 2.38 to 16.08), DQB1*0501 (OR, 6.16; 95% CI, 2.44 to 17.71), and DRB1*1501 (OR, 7.92; 95% CI, 2.71 to 23.14) were significantly increased in nonimmunosuppressed patients with PTB when compared with healthy subjects. By contrast, frequencies of allele DQB1*0402 and antigens DR4 and DR8 were significantly decreased in patients with PTB. Additionally, a significantly higher frequency of the DRB1*1101 allele was found in HIV-positive subjects (OR, 6.67; 95% CI, 2.13 to 20.83). Conclusion: The genetic influence associated with the HLA system appears to have an important role in the development of PTB, although this susceptibility may not be relevant in patients with severe immunodeficiency diseases such as AIDS. (CHEST 1999; 115: ) Key words: HIV; human leukocyte antigen; major histocompatibility complex; polymerase chain reaction; tuberculosis Abbreviations: CI confidence interval; CDC Centers for Disease Control and Prevention; EDTA ethylenediaminetetraacetic acid; HLA human leukocyte antigen; MHC major histocompatibility complex; OR odds ratio; PCR polymerase chain reaction; PTB pulmonary tuberculosis; SSPE sodium chloride, sodium phosphate, and EDTA; TB tuberculosis *From the Instituto Nacional de Enfermedades Respiratorias (Drs. Terán-Escandón, Terán-Ortiz, Camarena-Olvera, González-Avila, Vaca-Marín, and Selman) México DF, México; and the Instituto Nacional de la Nutrición Salvador Zubirán (Dr. Granados), Mexico City, México. Manuscript received March 30, 1998; revision accepted August 24, Correspondence to: Moisés Selman, MD, Instituto Nacional de Enfermedades Respiratorias Tlalpan 4502; Col. Sección XVI México DF, CP 14080, México; mselman@mailer.main. conacyt.mx Tuberculosis (TB) is still an important world health problem, and it is estimated that about one third of the earth s population has been infected with Mycobacterium tuberculosis. There are currently 8 million cases of active TB that cause 2.9 million deaths a year. 1 The disease rose to epidemic proportions with the advent of distressed environmental and socioeconomic conditions such as overcrowding, malnutri- 428 Clinical Investigations

2 tion, poor sewage disposal, and, more recently, the epidemic infection associated with HIV. 2 However, studies performed in humans and laboratory animals have strongly suggested that in addition to environmental factors, a genetic susceptibility may play a role in the development of the disease. 3,4 In this sense, it has been reported recently that variations in the gene encoding for the naturalresistance-associated macrophage protein 1 affect the susceptibility to TB of inhabitants of West Africa. 5 Since the major histocompatibility complex (MHC; human leukocyte antigen [HLA] system) plays an important role in the modulation of the immune response, a possible association between HLA antigens and TB has been examined in several populations, but the results have been controversial. 6 9 Discrepancies can be due to factors such as methodological problems, because studies have been done mostly with serologic techniques, which present cross-reactions and are considered to have low-grade specificity. 10 Moreover, serologic methods may produce erroneous designations of the HLA class II type in up to 25% of samples when compared with more sensitive molecular DNA-based methods. 11 In addition, susceptibility to TB is probably under multifactorial genetic control, including control by the HLA system. The HLA region is located in the short arm of chromosome 6, and it is separated into three subregions: the HLA class I region, encoding for HLA-A, -B, and -C antigens; the HLA class II region, encoding for HLA-DR, -DQ, and -DP antigens; and the HLA class III region, encoding for the second and fourth component of complement C2 and C4, factor B, tumor necrosis factors- and -, heat shock protein 70, and 21-hydroxylase. Class I and class II genes code for cell-surface glycoproteins whose function is to present antigenic peptides to CD8 and CD4 T cells, and play a fundamental role in the homeostasis of the immune response. 12 The HLA system is the most highly polymorphic biological system, and population differences are represented by the frequency of specific alleles and subtypes, and by the composition of extended haplotypes. The HLA system is a T cell restriction element closely related with immune-responsive and immune-suppressive genes. 13 Antigen-specific T cell responses require the presentation of processed peptides in association with MHC class I and class II cell-surface glycoproteins. In particular, proteins encoded by class II MHC genes function as restricting elements that mediate the recognition of the antigen by regulatory T cells and are closely associated with immune recognition and response. 14 The purpose of this study was to compare the frequency of HLA class II genes in adults with TB and in healthy control subjects by typing with a polymerase chain reaction (PCR). Additionally, HIVinfected patients with and without TB were examined. Study Population Materials and Methods Fifty randomly selected nonimmunosuppressed patients with pulmonary TB (PTB) were included in this study. The study subjects were unrelated Mexican patients who were residents of Mexico City and were hospitalized at the National Institute of Respiratory Diseases at the time of the study. In all cases, the diagnosis of TB was confirmed by light microscopy, which revealed the presence of acid-fast bacilli in sputum, and by culture of the M tuberculosis. The criteria for considering patients with TB as nonimmunosuppressed were the following: absence of HIV infection; normal lymphocyte and T lymphocyte count in peripheral blood; and confirmed lung infection by M tuberculosis. Patients with diabetes, silicosis, cirrhosis, or any systemic disease and patients who abused alcohol were excluded. AIDS patients with TB were analyzed independently. Evaluated as control subjects were 95 unrelated healthy individuals matched by ethnic and socioeconomic features, and 37 HIV-infected patients with neither PTB nor other infectious diseases (stage II in the Centers for Disease Control and Prevention [CDC] classification system for AIDS). 15 Additionally, 15 HIV-infected patients (AIDS CDC stage Ivc) with TB, and 20 healthy non-hiv-infected homosexual subjects were evaluated. HIV infection was diagnosed by enzyme-linked immunosorbent assay and was confirmed by Western blot analysis. Patients and control subjects were born in Mexico and displayed at least three generations of Mexican-born mestizo ancestors. The study was approved by the Scientific and Ethical Committees of our Institute, and signed consent was obtained from all individuals. Study Design DNA Extraction and Amplification: Genomic DNA from whole blood containing ethylenediaminetetraacetic acid (EDTA) was extracted by standard techniques. 16 DNA amplification and specific identification of HLA-DQ alleles were made by PCR using a PCR-specific sequence primer technique (Bio-Synthesis; Dallas, TX). Generic HLA-DRB1 typing was performed by using a PCR sequence-specific oligonucleotide probe hybridization reverse dot blot (Amplicor kit; Hoffman La Roche; Basel, Switzerland). DR1, DR2, DR4, DRB1-DR52, DRB3, and DRB5 amplifications were performed using a PCR with Taq polymerase (Promega; Madison, WI) as previously described. 17,18 The primers used for the amplification were DRBAMP-B for region 3 of exon 2 in all cases, and DRBAMP-1, DRBAMP-2, DRBAMP-3, DRBAMP-4, DRBAMP-5, and DRBAMP-52 for region 5 of exon 2 for each group of the specific amplification. They were synthesized in an automated synthesizer (DNA-SM; Beckman; Palo Alto, CA). Dot Blot Hybridization: Five percent of the amplified DNA was denatured in 0.4 mol/l NaOH for 10 min, was neutralized in 1 mol/l ammonium acetate, and was transferred to a membrane (Hybond-N; Amersham; Buckinghamshire, UK). The filters were prehybridized at 42 C for 30 min in a solution containing CHEST / 115 / 2/ FEBRUARY,

3 6 sodium chloride, sodium phosphate, and EDTA (SSPE; 30 SSPE [4.5 mol/l NaCl, 0.3 mol/l NaH 2 PO 4, 30 mmol/l EDTA, ph 7.4]), 5 Denhard s solution (2% bovine serum albumin, 2% polyvinylpyrrolidone 40, and 2% Ficoll 400), 0.1% lauryl-sarcosine, and 0.02% sodium dodecyl sulfate. Then, the oligonucleotide probes labeled with digoxigenin dideoxyuridine triphosphate were added and were hybridized at 42 C for 3 h. The filters were washed twice in 2 SSPE (ph 8.0, 3 mol/l tetramethylammonium chloride, 2 mmol/l EDTA, 0.1% sodium dodecyl sulfate) at room temperature for 10 min and twice at 60 C for 10 min. The dots were revealed using a nucleic acid detection kit (Dig Nucleic Acid Detection Kit; Boehringer Mannheim Biochemical; Mannheim, Germany). Oligonucleotide Probes: Information about the sequences and specificities of the DRB1, DRB3, DRB5, DQA1, and DQB1 oligonucleotides was obtained from the Twelfth International Histocompatibility Workshop (Paris, France). The oligonucleotide synthesis was made using the cyanoethyl phosphoramidite technique in an automated DNA synthesizer (DNA-SM; Beckman), following the manufacturer s protocol. Statistical Analysis After the phenotype frequencies were determined for each allele in the affected and control populations, the difference was established, and the statistical significance was proven by the 2 test with the Yates correction. A multiple polynomial logistic regression model using a computer program (STATA and Windows 95; Microsoft; Redmond, WA) was used to determine whether class II HLA alleles constitute a risk factor in the development of TB. 19 Odds ratios (ORs) were calculated with 95% confidence intervals (CIs). Results The study included 50 nonimmunosupressed patients (with a mean [ SD] age of years). Evaluated as control subjects were 95 healthy individuals ( years of age), 37 HIV-infected patients without infectious or neoplastic disease ( years of age), 15 immunosuppressed (HIV-infected) patients with TB ( years of age), and 20 healthy non-hiv-infected homosexual subjects ( years of age). The latter control group displayed no significant differences in HLA phenotypes when compared with a group of unrelated healthy individuals (data not shown). By using PCR and hybridization, significant allelic frequency differences were identified between nonimmunosuppressed patients with active TB and subjects in the other groups. The frequencies of each allele are shown in Table 1. Among the 50 nonimmunosuppressed patients with PTB, there were 30 patients with the DQA1*0101 allele, 22 with the DQB1*0501 allele, and 24 with the DRB1*1501 allele, compared with 20, 12, and 9 patients, respectively, from among the 95 healthy control subjects. The ORs for these alleles are shown in Table 2. The ORs of DQA1*0101 and DQB1*0501 from the DQ1 chain were 6.18 (95% CI, 2.38 to 16.08) and 6.16 (95% CI, 2.44 to 17.71), respectively. At the HLA-DR2 locus, the frequency of the DRB1*1501 allele was significantly increased, exhibiting an OR of 7.92 (95% CI, 2.71 to 23.14). No disequilibrated haplotypes between the DR and DQ loci were found in the PTB patients. Additionally, HIV-positive patients revealed a significant increase in the frequency of the DR5 allele DRB1*1101 (OR, 6.67; 95% CI, 2.13 to 20.83; Table 2). On the other hand, three alleles were associated with a reduced risk of developing PTB. Thus, the frequencies of the DQB1*0402 allele from locus DQ and the DR4 and the DR8 alleles from locus HLA- DR, were significantly decreased in patients with PTB with ORs of 0.18 (95% CI, 003 to 0.92), 0.24 (95% CI, 0.07 to 0.84), and 0.10 (95% CI, 0.01 to 0.74), respectively. Discussion Molecular typing has proven useful for clarifying the genetic susceptibility associated with the HLA system. Tissue or cell sampling may now be achieved by examining the cell nucleic acid rather than by using serologic methods, thus increasing the sensitivity of the sampling. In our study, PCR, in combination with the sequence-specific oligonucleotide probes, clearly showed an association between the frequencies of the DQA1*0101, DQB1*0501, and DRB1*1501 alleles and PTB. The aforementioned markers were increased independently, and no haplotypes could be defined. Interestingly, AIDS patients with PTB did not show any of these relationships, suggesting that the severe acquired immunosuppressive state predisposes individuals to the development of TB despite the lack of genetic susceptibility. However, the size of this group was too small to reach any conclusion, and further studies with a larger group of patients who have AIDS and PTB are necessary. Additionally, the frequencies of some HLA alleles from the DR and DQ loci were found to be significantly increased in healthy control subjects compared to HLA alleles in PTB patients, suggesting that those alleles may confer some resistance to this infectious disease. A recent study performed using PTB patients from India demonstrated an association with the HLA- DR2 antigen, but the bulk of the alleles were DRB1*1501 and DRB1*1502 both in patients and control subjects. 20 In the same study, molecular subtyping of the DQ allele was not performed. More recently, an association of HLA-DQB1*0503 and clinical TB was found in Cambodian patients. 21 In this study, only a slight increase of HLA-DR2 antigen was noticed. 430 Clinical Investigations

4 Table 1 The Frequency of the HLA Class II Alleles in the Four Groups Allele Specificity Healthy Subjects, % PTB Patients, % HIV-Positive Patients, % AIDS Patients with PTB, % DR DR DR DR DR DR DR DR11 (DRB1*1101) (DRB1*1102) (DRB1*1103) (DRB1*1104) DR12 (DRB1*1201) (DRB1*1202) (DRB1*1203) DR13 (DRB1*1301) (DRB1*1302) (DRB1*1305) DR DR15 (DRB1*1501) (DRB1*1502) (DRB1*1503) DR16 (DRB1*1601) (DRB1*1602) DQA (DQA1*0101) (DQA1*0102) (DQA1*0201) (DQA1*0301) (DQA1*0401) (DQA1*0501) (DQA1*0502) DQB (DQB1*0201) (DQB1*0301) (DQB1*0302) (DQB1*0304) (DQB1*0402) (DQB1*0501) (DQB1*0502) (DQB1*0503) (DQB1*0504) (DQB1*0602) (DQB1*0603) (DQB1*0604) (DQB1*0609) p when compared with the healthy control group. The HLA-DQ molecules are unique among class II MHC molecules because both the - and -chains are highly polymorphic; furthermore, most of the variable amino acid residues are located on the -helical part of the antigen-binding site. 22 In our study, PCR analysis of the DQ allele revealed two subtypes strongly associated with TB. To a great extent, risk factors associated with the development of pulmonary and extrapulmonary diseases are environmental and are primarily the result of exposure to M tuberculosis. However, the factors that influence the development of the disease and its clinical behavior are not completely understood. In general, among individuals exposed to M tuberculosis, not all become infected, and among those infected the progression to active disease, the course of CHEST / 115 / 2/ FEBRUARY,

5 Table 2 Alleles Associated With Increased Risk for Development of TB Alleles PTB Patients HIV-Positive Patients AIDS Patients with PTB DQA1*0101 OR % CI DQB1*0501 OR % CI DRB1*1501 OR % CI DRB1*1101 OR % CI the disease, and its duration are highly variable. Most likely, a complex interaction of genetic and environmental factors is operative. It is well known that distressed environmental conditions and some identifiable risk factors such as diabetes, silicosis, AIDS, and alcohol abuse, among others, play a role. In this context, family income and nutritional status, known cofactors for the development of TB, were similar between PTB patients and healthy control subjects; likewise, patients with some of the mentioned disorders were ruled out of the PTB group, and AIDS patients with TB were analyzed independently. Host genetic factors may also influence both susceptibility to infectious agents and their associated disease pathogenesis, although evidence for genetic susceptibility to TB in humans has been difficult to obtain. Recently, it was found that variation in the human macrophage protein 1, which is associated with natural resistance, is associated with altered susceptibility to smear-positive TB in inhabitants of West Africa. 5 Our results and those reported by Goldfeld et al 21 support the notion that some alleles of the class II HLA system, mainly those belonging to the locus DQ1, could participate in increasing susceptibility to the development of TB. The HLA-restricted presentation of processed antigens by alveolar macrophages may be affected in patients who express these particular alleles. An additional finding of the present work was the increase in frequency of the DRB1*1101 allele in HIV-infected patients. Interestingly, by using standard microcytotoxicity methods on mononuclear cells, the high frequency of the HLA-DR5 antigen was reported some years ago in AIDS patients. However, it was unclear whether the HLA-DR5 antigen predisposed patients to the development of AIDS or to some subsequent complications, such as persistent generalized lymphadenopathy and Kaposi s sarcoma Since the frequency of the DRB1*1101 allele was significantly increased in CDC stage II HIV infection, our results suggest that the genetic susceptibility associated with this marker seems to predispose patients to the HIV infection rather than to the ensuing complications. In support of this viewpoint, class II HLA typing in 20 male homosexual subjects without HIV infection showed that the frequency of the DRB1*1101 allele in these individuals is similar to that of the control groups (not shown). However, this finding needs to be considered cautiously because, despite many studies concerning the host HLA type and the immune response of HIV-1, the question of whether HLA influences susceptibility to this viral infection remains unresolved. 26 In summary, our findings suggest that three alleles confer susceptibility to the development of PTB in the Mexican population. The underlying mechanisms of HLA class II disequilibria and susceptibility to infectious diseases, as well as the differences between the DR and DQ loci disequilibria, are still unknown. However, our results suggest that a genetic influence associated with this system may play a role in the development of TB but that this putative susceptibility may not be relevant in patients with severe immunodeficiency diseases such as AIDS. Additionally, a subtype of the DR5 antigen might be associated with the development of HIV infection. References 1 Kochi A. The global TB situation and the new control strategy of the World Health Organization. Tubercle 1991; 72:1 6 2 Centers for Disease Control. TB and human immunodeficiency virus infection: recommendation of the Advisory Committee for Elimination of TB. MMWR 1989; 38: Todd JR, West BC, MacDonald JC. HLA and leprosy: study in Northern Louisiana and review. Rev Infect Dis 1990; 12: Skamene E. Genetic control of susceptibility to mycobacterial infections. Rev Infect Dis 1989; 11(suppl 2):394S 399S 5 Bellamy R, Ruwende C, Corrah T, et al. Variations in the NRAMPI gene and susceptibility to TB in West Africans. N Engl J Med 1998; 338: Sanjeevi CB, Narayanan PR, Prabakar R, et al. No association or linkage with HLA-DR or DQ genes in South India with pulmonary TB. Tubercle 1992; 73: Bothamley GH, Beck JS, Schreuder GMT, et al. Association of TB and M: TB-specific antibody levels with HLA. J Infect Dis 1989; 159: Khomenko AG, Litvinov VI, Chukanova VP, Pospelov LE. TB in patients with various HLA phenotypes. Tubercle 1990; 71: Pospelov LE, Matrakshin AG, Chernousova LN, et al. Association of various genetic markers with TB and other lung diseases in Tuvinian children. Tubercle Lung Dis 1996; 77: Clinical Investigations

6 10 Trowsdale J, Powis S, Campbell D. The contribution of novel MHC genes to disease. In: HLA and disease. San Diego, CA: Academic Press; 1994: Opelz G, Mytilineos J, Scherer S, et al. Survival of DNA HLA-DR types and matched cadaver kidney transplant. Lancet 1991; 338: Accolla RS, Adorini L, Sartoris S, et al. MHC: orchestrating the immune response. Immunol Today 1995; 16: Benacerraf B. Role of MHC gene products in immune regulations. Science 1981; 212: Takahara N. MHC diversity and selection. Immunol Rev 1995; 143: Centers for Disease Control. Revision of the CDC surveillance case definition for acquired immunodeficiency syndrome. MMWR 1987; 36:15 16 Davis RW, Thomas M, Cameron J, et al. Rapid DNA isolation for enzymatic and hybridization analysis. Methods Enzymol 1980; 65: Jordan F, McWhinnie AJ, Turner S, et al. Comparison of HLA-DRB1 typing by DNA-RFLP, PCR-SSO and PCR-SSP methods and their application in providing matched unrelated donors for bone marrow transplantation. Tissue Antigens 1995; 45: Corell A, Martin-Villa JM, Varela P, et al. Exon 2 DNA sequence of the Drw 13b allele obtained from genomes of five different individuals Mol Immunol 1990; 27: Hosmer DW, Lemeshow S. Applied Logistic Regression. New York, NY: John Wiley & Sons, 1989; Rajalingam R, Mehra NK, Jain RC, et al. Polymerase chain reaction-based sequence-specific oligonucleotide hybridization analysis of HLA class II antigens in pulmonary TB: relevance to chemotherapy and disease activity. J Infect Dis 1996; 173: Goldfeld AE, Delgado JC, Thim S, et al. Association of an HLA-DQ allele with clinical TB. JAMA 1998; 279: Marsh SGE, Bodmer JG. HLA-DR, and -DQ epitopes and monoclonal antibody (MoAb) specificity. Immunol Today 1989; 10: Enlow RW, Nuñez Roldan A, LoGalbo P, et al. Increased frequency of HLA-DR5 in lymphadenopathy stage of AIDS. Lancet 1983; 2: Smeraldi RS, Lazzarin A, Moroni M, et al. HLA-associated susceptibility to acquired immunodeficiency syndrome in Italian patients with human-immunodeficiency-virus infection. Lancet 1986; 2: Rafoux C, David V, Couderc LD, et al. HLA-A.B and DR antigen frequencies in patients with AIDS-related persistent generalized lymphadenopathy (PGL) and thrombocytopenia. Tissue Antigens 1987; 29: Just JJ. Genetic predisposition to HIV-1 infection and acquired immune deficiency virus syndrome: a review of the literature examining associations with HLA. Hum Immunol 1995; 44: CHEST / 115 / 2/ FEBRUARY,

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