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Mitochondrial Diseases

Mitochondrial diseases are a group of disorders relating to the mitochondria, the organelles that are the "powerhouses" of the eukaryotic cells that comprise higher-order lifeforms (including humans). The mitochondria convert the energy of food molecules into the ATP that powers most cell functions. more...

Mac Ardle disease
Macular degeneration
Mad cow disease
Maghazaji syndrome
Mal de debarquement
Malignant hyperthermia
Mallory-Weiss syndrome
Malouf syndrome
Marburg fever
Marfan syndrome
MASA syndrome
Mast cell disease
MAT deficiency
Maturity onset diabetes...
McArdle disease
McCune-Albright syndrome
Mediterranean fever
Megaloblastic anemia
Meleda Disease
Meniere's disease
Mental retardation
Mercury (element)
Metabolic acidosis
Metabolic disorder
Methylmalonic acidemia
Microscopic polyangiitis
Microtia, meatal atresia...
Miller-Dieker syndrome
Mitochondrial Diseases
Mitral valve prolapse
Mobius syndrome
MODY syndrome
Moebius syndrome
Molluscum contagiosum
MOMO syndrome
Mondini Dysplasia
Mondor's disease
Monoclonal gammopathy of...
Morquio syndrome
Motor neuron disease
Moyamoya disease
MPO deficiency
Mullerian agenesis
Multiple chemical...
Multiple endocrine...
Multiple hereditary...
Multiple myeloma
Multiple organ failure
Multiple sclerosis
Multiple system atrophy
Muscular dystrophy
Myalgic encephalomyelitis
Myasthenia gravis
Mycosis fungoides
Myelodysplastic syndromes
Myeloperoxidase deficiency
Myoadenylate deaminase...
Myositis ossificans

Mitochondrial diseases comprise those disorders that in one way or another affect the function of the mitochondria and/or are due to mitochondrial DNA. Mitochondrial diseases take on unique characteristics both because of the way the diseases are often inherited and because that mitochondria are so critical to cell function. The subclass of these diseases that have neuromuscular disease symptoms are often referred to as a mitochondrial myopathy.

Mitochondrial inheritance

Mitochondrial inheritance behaves differently from the sort of inheritance that we are most familiar with. Regular nuclear DNA has two copies per cell (except for sperm and egg cells). One copy is inherited from the father and the other from the mother. Mitochondria, however, contain their own DNA, and contain typically from five to ten copies, all inherited from the mother (for more detailed inheritance patterns, see mitochondrial genetics). When mitochondria divide, the copies of DNA present are divided randomly between the two new mitochondria, and then those new mitochondria make more copies. As a result, if only a few of the DNA copies inherited from the mother are defective, mitochondrial division may cause most of the defective copies to end up in just one of the new mitochondria. Once more than half of the DNA copies are defective, mitochondrial disease begins to become apparent, this phenomenon is called 'threshold expression'.

It should be noted, however, that not all of the enzymes and other components necessary for proper mitochondrial function are encoded in the mitochondrial DNA. Most mitochondrial function is controlled by nuclear DNA instead.

To make things even more confusing, mutations to mitochondrial DNA occur frequently, due to the lack of the error checking capability that nuclear DNA has. This means that a mitochondrial disorder can occur spontaneously rather than be inherited. Further, sometimes the enzymes that control mitochondrial DNA duplication (and which are encoded for by genes in the nuclear DNA) are defective, causing mitochondrial DNA mutations to occur at a rapid rate.

Defects and symptoms

The effects of mitochondrial disease can be quite varied. Since the distribution of defective DNA may vary from organ to organ within the body, the mutation that in one person may cause liver disease might in another person cause a brain disorder. In addition, the severity of the defect may be great or small. Some minor defects cause only "exercise intolerance", with no serious illness or disability. Other defects can more severely affect the operation of the mitochondria and can cause severe body-wide impacts. As a general rule, mitochondrial diseases are worst when the defective mitochondria are present in the muscles or nerves, because these are the most energy-hungry cells of the body.


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Mitochondrial DNA Variations in Russian and Belorussian Populations
From Human Biology, 10/1/03 by Belyaeva, Olga

Abstract The sequence of the first hypervariable segment (HVS-I) of mitochondrial DNA (mtDNA) was determined in 251 individuals from three eastern Slavonic populations, two Russian and one Belorussian. Within HVS-I, 78 polymorphic positions were revealed. Within-population diversity of HVS-I varies slightly among three samples; its estimates do not differ strongly from those for European populations. Haplotype diversity for three populations calculated in this study is 0.949; mean pairwise differences estimate is 3.59. To assign mtDNA sequences to major phylogenetic clusters, haplogroup-specilic restriction polymorphisms were selectively typed in most samples. The haplogroup distribution in the total Eastern Slavonic sample is similar to that reported for the European sample. However, the separate consideration of three Slavonic samples reveals the complicated structure of the mitochondrial gene pool in the Eastern European area. Data of this study support the proposed model of the origin of modern Eastern Slavs, which implies the admixture of ancient Slavonic tribes with pre-Slavonic populations of Eastern Europe. These data should contribute to general studies of mitochondrial DNA variations in Europe.


European mitochondrial DNA (mtDNA) diversity, despite its comparatively low level, is widely employed in studies of origin and evolution of maternal lineages. Detailed studies were performed to describe mtDNA variations in separate populations as well as to reveal general tendencies in the process of the colonization of Europe, which contributed to the modern European mitochondrial gene pool formation. The identification of phylogenetic mtDNA clades, or haplogroups, and analysis of their distribution were successfully used to reveal the continent-wide mitochondrial variation pattern and to trace prehistoric migrations during the colonization of Europe (Richards et al. 1998; Macaulay et al. 1999; Simoni et al. 2000; Torroni et al. 2001; Richards et al. 2000). Recently, studies in several populations revealed that particular haplogroups could also be associated with longevity and diseases (Torroni et al. 1997; De Benedictis et al. 1999; Rose et al. 2001). Slavonic and, in particular, Eastern Slavonic populations, which inhabit a large part of the Eurasian territory, were significantly underrepresented in mtDNA diversity studies. Recently, data on coding and control region mtDNA variations and haplogroup distribution in several Russian, one Ukrainian, and one Polish samples were reported (Orekhov et al. 1999; Maliarchuk and Derenko 2000; Malyarchuk et al. 2002) and implicated to the question of origin of the Eastern Slavs (Malyarchuk and Derenko 2001). Here we present data on mtDNA polymorphism in three other native population samples belonging to two Eastern Slavonic peoples, Russians and Belorussians.

Materials and Methods

Populations Studied. Population samples were collected after obtaining informed consent according to the following criteria: all individuals belong to the native population of the regions studied (at least three female generations living in the region), they are maternally unrelated, and they are of Slavonic origin (Russian or Belorussian, depending on the sample). The Belorussian sample (92 individuals) was collected in Bobruisk, located in the central part of the Republic of Belarus. Two Russian samples represent a native rural population of two geographically distant regions of the Russian Plain. The first one (76 individuals) was collected in the settlement of Oshevensk in the Arkhangelsk region of northern Russia. This settlement is situated in the Kargopol district, in the southernmost part of the Arkhangelsk region, which was colonized during the very early period of the formation of the Russian State. Its isolated rural populations are supposed to be little affected by recent migrations and are very interesting with respect to genetic studies. The second sample (83 individuals) was collected in Bashkiria, Arkhangelsky district, but includes only ethnically Russian individuals. The Russian population of the Ural region, to which Bashkiria belongs, was formed mostly by migrants from southern areas of the country, and is supposed to differ genetically from the northern population.

Hypervariable Segment I Polymorphism Analysis. DNA was isolated from peripheral blood according to the standard phenol-chloroform extraction protocol. The first hypervariable segment (HVS-I) fragment of the mitochondrial control region was amplified by polymerase chain reaction (PCR) using primers con E2 (5'-CAC CAT TAG CAC CCA AAG CT-3') and con H2-B (5'-TGA TTT CAC GGA GGA TGG TG-3') (Richards et al. 1996). Amplicons were sequenced in both directions by use of the Sanger dideoxy-chain-termination method and cycle-sequencing protocol with [[lambda]-^sup 33^P]-labeled amplification primers. PCR and cycle sequencing reactions were performed in an MJR ptc-100 thermal cycler (MJ Research, MA, USA). Sequences were determined between positions 16040 and 16365 (Anderson et al. 1981). Positions different from the Cambridge reference sequence (CRS, Anderson et al. 1981) were identified. Simple haplotype diversity, h, estimated by the method of Nei (Nei 1987), and mean pairwise differences were determined using DnaSP version 3.53 software (Rozas et al. 1999). The standard error of mean pairwise differences was estimated from 200 bootstrap replications of the primary data set.

Restriction Fragment Length Polymorphism Analysis and Haplogroup Assignment. In some cases, haplogroup assignment of mtDNA sequences could be performed on the basis of diagnostic HVS-I motifs (Macaulay et al. 1999; Richards et al. 2000). For those lineages that do not have a distinctive HVS-I motif, or in which this motif is ambiguous, additional coding-region restriction fragment length polymorphism (RFLP) markers were typed to confirm or exclude the affiliation with a particular haplogroup. In this study, selective RFLP polymorphisms were analyzed in most individual samples. To determine the RFLP status of mitochondrial sequences, restriction endonuclease analysis was performed on mtDNA fragments amplified as described by Torroni et al. (1996, 1997). The 7025AluI site was tested to reveal haplogroup H sequences (-7025AluI). Those +7025AluI samples lacking the 14766Mset site were identified as belonging to the HV cluster; from them, sequences bearing 16298C substitution on the HV background were identified as pre-V. In +7025AluI, +14766Mset sequences, the 12308HinfI site was tested to identify haplogroup U (+12308HinfI). Within haplogroup U, sequences were assigned to subclusters on the basis of HVS-I diagnostic motifs, as was done within haplogroups J and T. In cases of ambiguous sequence motif, affiliation with haplogroup T was determined by +13366BamHI. 10394Ddel, 10397AluI sites were typed in all 16223T samples. The +10394DdeI, + 10397Alu status was used as a marker of haplogroup M; +14465AccI was used as a marker of haplogroup X; and +10028AluI, +16389BamHI was used as a marker of haplogroup I. Haplogroups W, C, and N were identified on the basis of HVS-I sequence (Macaulay et al. 1999). Lineages that could not be assigned using HVS-I sequence motif and the restriction markers mentioned above were named "Other." The comparison of haplogroup distribution among samples was performed using POPGENE software version 1.32 (Yeh et al. 1997).

Results and Discussion

HVS-I Sequence Variability. We performed the sequence analysis of the first hypervariable segment of the mitochondrial D-loop in three different Slavonic samples, two Russian and one Belorussian. Mitochondrial DNA of 251 individuals was analyzed, including 92 Belorussian individuals from Bobruisk, 76 and 83 Russian individuals from Arkhangelsk region (Oshevensk) and Bashkiria, respectively.5

The total number of HVS-I polymorphic sites revealed in the three populations is 78 (data on sequence variations and their distribution are presented in the Table 1). Most of them are transitions. Of the total number of substitutions in Russians (Bashkiria), 5 (11.1%) are transversions, versus 2 (4.4%) transversions in Russians (Oshevensk) and 3 (5.4%) transversions in Belorussians.

For HVS-I variations, the simple haplotype diversity was determined as a measure of within-population genetic diversity. It shows relatively high values, with the estimate 0.95 for three samples in total and the highest value for the northern Russian population (Table 2). Mean pairwise difference estimates, relatively low, range between 3.33 and 3.80, also reaching the highest value in Russians (Oshevensk). Thus, all three Slavonic samples show high estimates of haplotype diversity combined with low values of mean pairwise differences, which is typical for European mitochondrial DNA diversity described elsewhere. The Russian (Oshevensk) sample shows slightly higher haplotype diversity and number of mean pairwise differences than the two other samples.

The percentage of unique HVS-I haplotypes has the lowest value (68.3%) in Russians (Oshevensk) and the highest (84.6%) in Russians (Bashkiria). These estimates show that the female population of Oshevensk represents a more restricted pool than those of the two other Slavonic samples. The percentage of unique haplotypes estimated for the three populations in total (77.3%) is close to the estimate of approximately 77% for the European population (Richards et al. 1996). This finding suggests that treating Russians as one total population, as has been done in earlier studies, could mask significant heterogeneity and differences among local groups.

HVS-I and RFLP Combined Data. In addition to the sequence analysis, major haplogroup-defining RFLP markers were typed selectively in those samples that could not be assigned to any cluster on the basis of a diagnostic HVS-I motif. The HVS-I and RFLP typing revealed 139 different lineages (Table 1).

A relatively high number of lineages in Russians from Bashkiria ("Other," 15.7%; Table 3) was not assigned to any group. HVS-I and determined RFLP markers (+7025AluI, +14766Mset, -13366BamHI, -12308HinfI, and also -10397AluI, -10394Ddel for 16223T-sequences) imply that most probably these lineages belong to pre-HV or other clusters encompassed by R (Macaulay et al. 1999), excluding HV, U, and JT. At the least, the status of the 00073 position should be determined in assigning these sequences, but 00073 typing was not performed in this study.

The most abundant HVS-I type in all populations was CRS. Additional RFLP typing performed on these sequences revealed the heterogeneity of this group. Interestingly, a relatively high proportion of CRS sequences belongs to haplogroup U (+12308HinfI). In Belorussian and Russian (Bashkiria) populations it constitutes 33.3% and 36.8% of CRS lineages, correspondingly. Data from earlier studies reported that within Europe CRS lineages were assigned predominantly to haplogroup H (Richards et al. 2000). Haplogroup H constitutes the majority of all three samples analyzed in this study, a finding similar to those for other European and Middle Eastern groups (Richards et al. 1998, 2000), as well as to those for previously reported Slavonic samples (Orekhov et al. 1999; Malyarchuk and Derenko 2001; Malyarchuk et al. 2002). Two 16223T substitutions were observed among haplogroup H sequences, one in each Russian sample. Sequences bearing 16223T substitutions on the haplogroup H background were described also in another Slavonic sample, Ukrainians (Malyarchuk and Derenko 2001). As mentioned by the authors of this study, this substitution is rare among European sequences not belonging to I, W, or X groups. In addition, five more 16223T sequences observed in Russians (Bashkria) were assigned to "Other" and do not belong to M, I, W, or X clusters. A high representation of 16240C sequences could be mentioned as another peculiarity of haplogroup H in the northern Russian population. This rare substitution, also reported by Helgason et al. (2001) in a Scottish sequence, was observed in seven maternally unrelated individuals, five of them bearing the single 16240C transversion, and in two sequences representing probable derivatives.

The distribution of haplogroup pre-V in our samples could be of some interest, because in studies of Torroni et al. (1998, 2001) a postglacial recolonization of Europe and population expansion from southwestern to northeastern Europe was inferred from the haplogroup V distribution. Pre-V lineages have equally significant frequencies (5.4% and 5.3%) in Belorussians and Russians (Oshevensk), while in Russians (Bashkiria) this cluster is represented by a single individual sequence. This observation is consistent with the higher frequency of V in northern European populations.

Significant differences were noted in the representation of the HV monophyletic cluster. While more than half of individual lineages in Belorussians and Russians (Oshevensk) belong to this cluster, the population of Russians (Bashkiria) demonstrates the decreased level of 32.5%.

Haplogroup U sequences are widely distributed in the Eastern Slavonic samples described here. Their frequency in both Russian samples is higher than in the Russian sample reported by Malyarchuk and Derenko (2001) (28.6% and 26.3%, against 14.0%), though closer to the frequency in the Russian sample from the Malyarchuk et al. (2002) study (20%). In Russians (Bashkiria) haplogroup U has higher diversity than in two other samples, with a greater number of different subclusters. As mentioned above, one unusual feature of haplogroup U in the two Eastern Slavonic populations consists of a high content of CRS lineages. Also unlike findings for earlier reported Slavonic samples, haplogroup K has a significant frequency (7.9%) in the northern Russian population, but is rare in Belorussians and Russians (Bashkiria). U5, the most ancient European subcluster of U, is well represented in all three samples with frequencies close to the European average (Richards et al. 2000). The presence of the U5b1 subcluster in the northern Russian population should also be noted. U5b1 sequences in Russians were also reported by Malyarchuk et al. (2002). This subcluster was described as specific for the Saami population (Lahermo et al. 1996). Its presence in the Russian (Oshevensk) sample seems to reflect an admixture of a Finno-Ugric component, but it is unclear how old this admixture could be. All individuals included in our sample were characterized as ethnically Russian, and inhabited the area where the sample was collected for at least three maternal generations. Currently, due to geographical and sociological peculiarities, the Russian population of the Oshevensk settlement can be considered an isolate. The southern part of the Arkhangelsk region, where the Oshevensk settlement is situated, does not have immediate contact with Saami populations. So, a recent admixture seems to be less probable than an earlier admixture during the peopling of northern areas by Slavonic groups.

Haplogroup J shows a significant diversity in our Slavonic samples and includes five different subclusters, in contrast to Russian samples reported earlier, where / sequences were represented mostly by 16069T-16126C types. Haplogroup T is also diversified and occurs at a significant level in Belorussians and Russians (Oshevensk), but is less frequent in Russians (Bashkiria).

European-specific haplogroups I, W, and X are rare, with the exception of Russians (Bashkiria), where I contains four individual sequences.

In comparison to frequencies of cluster M in Belorussians and the northern Russian population, the frequency of cluster M in Russians (Bashkiria) is notably but not dramatically increased (five sequences). Although we collected samples from individuals who are ethnically Russian for at least three generations, we cannot exclude the possibility of some admixture with neighboring Asian populations characterized by high frequencies of the cluster M. In the meantime, those undetermined "Other" sequences, which contain the 16223T motif (six individuals), were tested for 10397AM and 10394DdeI status. Because they lack restriction sites at these positions, however, this portion of the "Others" group could not contribute to the cluster M in Russians (Bashkiria). Thus, this population differs remarkably in the distribution of haplogroups within cluster R (Macaulay et al. 1999). Therefore, only the recent admixture, to which Russians (Bashkiria) are more exposed geographically, cannot easily explain the differences between this population and two others.

Conclusions. As follows from the above discussion, three eastern Slav samples considered in total demonstrate mtDNA variations that are very close to variations found in the European population as a whole. MtDNA haplotypes are similar to those found in Western and Central European populations. Nevertheless, the comparison of Slavonic samples of different ethnic and geographic origins reveals the complicated structure of the mitochondrial gene pool in this area. This structure could reflect traces of female admixture between Slavonic and pre-Slavonic groups-in particular, Finno-Ugric tribes-during a colonization of northern Eastern Europe by Slavs. In this sense our data are in agreement with those from previous studies of Slavonic mtDNA (Malyarchuk and Derenko 2001) and a hybridization theory of the origin of Eastern Slavs (Alekseeva 1973), which imply their central European origin and subsequent admixture and assimilation of pre-Slavonic populations of Eastern Europe. This study also revealed no or low Mongoloid admixture in the mitochondrial gene pool of Eastern Slavs. However, the analysis of maternally inherited mtDNA could not effectively reveal the influence of Mongoloid migrations, since they included mostly male individuals. Haplogroup distribution in Belorussians and northern Russians has more similarity to that in northern European populations than in eastern Russian populations. The Russian (Bashkiria) population differs from the two other samples in the representation of several clusters, namely, HV, V, K, T. Besides the local admixture and assimilation of pre-Slavonic groups, this difference could support an existing opinion that Russian migrants of different geographic origin were involved in the processes of colonizing the northern and eastern parts of the Russian Plain. More detailed studies of Eastern European mtDNA variations, complemented by analysis of Y-chromosome loci, will allow revelation of some tendencies, which could reflect the main aspects of European gene pool formation.

Acknowledgments This work was partially supported by the Russian Art and Scientific Foundation and the Russian Basic Research Foundation.

5 Sequence variants corresponding to HVS-I haplolypes determined in this study were deposited in the GenBank(TM) under accession numbers AY005336-AY005390 (Belorussian sample), AY005827-AY005866 (Russians, Oshevensk) and AF292943-AF292943 (Russians, Bashkiria).

Received 21 January 2003; revision received 28 April 2003.

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1 Institute of Molecular Genetics of RAS, Moscow, Russia.

2 Institute of Biochemistry and Genetics, Ufa Science Center of RAS, Ufa, Russia.

3 Arkhangelsk State Medical Academy, Arkhangelsk, Russia.

4 Institute of Ethnography and Anthropology, Minsk, Republic of Belarus.

Copyright Wayne State University Press Oct 2003
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