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IMPORTANCE OF PURIFICATION

OF HEPATIC CYTOCHROME P-450

FOR STUDYING DRUG METABOLISM

IN MAN

R. KATO & T. KAMATAKI

Department ofPharmacology, School ofMedicine,

Keio University, Tokyo, Japan

In the past decade, efforts made by severallaboratories have created much progress in

the purification of cytochrome P-450. These studies have provided useful information which should be considered by clinical pharmacologists, in human therapy.

The most meaningful information obtained is that there are multipleforms of

cytochrome P-450 in liver microsomes. Thus, the pharmacological significance of

the multiple forms ofcytochrome P-450 will be discussed.

Multiple forms of cytochrome P-450 in experimental animals

There has been a great number of reports suggesting the presence of at least two

forms of drug metabolizing enzymes in liver microsomes of experimental animals.

For example, treatment of rats with phenobarbitone induces a wide variety of drug

metabolizing activities while treatment with polycyclic hydrocarbons, such as

3-methylcholanthrene, induces only limited activities. The difference in the drug

metabolizing activities were later proved to be caused by the presence of different

forms of cytochrome P-450 in these induced microsomes (Kuntzman, Lu, West,

Jacobson & Conney, 1971; Lu & Levin, 1974; Ryan, Lu, Kawelek, West & Levin,

1975). The purified preparations showed substrate specificities for the oxidations of

benzo[a]pyrene, benzphetamine and other drugs, Thereafter, the presence ofmultiple

forms of cytochrome P-450, which are distinguishable in their catalytic activities, in

molecular weight, in physical property during purification, in amino acid sequence

and in immunological cross reactivity between each form of purified cytochrome

P-450 and the antibody, were suspected. Up to date , the presence of eight forms of

cytochrome P-450 in rabbits and at least four forms of cytochrome P-450 in rat liver

microsomes have been postulated and some of these forms were purified and

partially characterized (Levin, 1977; Guengerich, 1979). The substrate specificity of

the purified cytochrome P-450 is in contrast to the classical concept of the drug

metabolizing enzyme , since a drug metabolizing enzyme having a quite broad

substrate specificity had been believed to be involved in metabolizing a wide variety

ofdrugs consisting ofeven newly synthesized drugs.

PURIFICATION OF HEPA TIC CYTOCHROME P-450

Multiple forms of cytochrome P-450 in human Iiver microsomes

81

The presence of cytochrome P-450 in human liver microsomes was first demonstrated spectrophotometrically by Alvares, Schilling, Levin, Kuntzman, Brand &

Mark (1969). As reviewed by Pelkonen, Haltiala, Larmi & Karki (1974), the specific

content of cytochrome P-450 in human liver microsomes has been reported to vary

from one individual to another, probably depending upon the freshness of the

sampie, cause of death, intake of drugs, and so on. The purification of cytochrome

P-450 from human microsomes was first tried by Kaschnitz & Coon (1975). Purification from an autopsy sampie, was performed, to a specific content of0.42 nmol mg

protein-I and it was demonstrated that the human cytochrome P-450 was capable of

catalyzing ethylmorphine N-demethylation, requiring a phospholipid for the

activity. Human cytochrome P-450 was purified in this laboratory, to a specific

content of 10.6 nmol mg protein-', the purified preparation apparently showed a

single band on SDS-polyacrylamide gel electrophoresis, with a molecular weight of

approximately 53 ,800 and was active for drug oxidations when cumene hydroperoxide was used as an oxygen donor (Kamataki, Sugiura, Yamazoe & Kato, 1979).

To examine further the properties of human cytochrome P-450, Wang, Mason &

Guengerich (1980) purified, from autopsy sampies, a form of cytochrome P-450 to

homogeneity with a specific content ofl4 nmol mg proteirr",

As mentioned above, the presence of multiple forms of cytochrome P-450 was

confirrned in experimental animals. Thus, it is reasonable to assurne that multiple

forms are also present in human microsomes and that they oxidize numerous

endogenous and exogenous compounds. The difficulty in purification ofthe multiple

forms from human liver was due mainly to the type of sample available. When an

autopsy sampie, wh ich was most readily available, was used, a minor or unstable

form ofcytochrome P-450 might have been degraded before starting purification, To

minimize such degradation of the cytochrome after death, Beaune, Remers &

Dansette (1980) employed livers from kidney transplantation donors immediately

after death, to separate three fractions containing cytochrome P-450. The purified

preparations were distinguishable in their catalytic activities. Although furt her

characterization is needed, their fmding was the first evidence showing that there are

multiple forms of cytochrome P-450 in human livers. To further support this, two

forms of cytochrome P-450, from autopsy sampies were recently purified in our

laboratory. Human microsomes were solubilized by sodium cholate, then

cytochrome P-450 was precipitated by polyethylene glycol 6,000. The polyethylene

glycol precipitates were applied to a w-amino-n-octyl Sepharose 4B column.

Cytochrome P-450 was eluted from the column using Emulgen 911 as an inhibitor.

The fractions containing cytochrome P-450 were passed through a DEAE-cellulose

(DE-52) column and then applied to a CM-Sephadex (C-50) column. A majority of

cytochrome P-450 which did not adsorb on the CM-Sephadex column was applied

to a hydroxylapatite column. The cytochrome P-450 was eluted from the column by

increasing the phosphate concentration. This cytochrome P-450 preparation was

designated as Form 1.Cytochrome P-450 adsorbed on the CM -Sephadex column was

eluted by 500 mM potassium phosphate (pH 7.25) containing 20% glyceroI. This

cytochrome P-450 preparation was designated as Form ll . The specific contents of

Form 1 and Form Il were 15.2-16.8 and 6.8-9.0 nmol mg protein-I, respectively.

These two forms still contained a protein as a contaminant but were distinguishable

in their molecular weights (Figure I) and in their catalytic activities (Table I). These

results were then compared with those ofBeaune et a/. (1980) and those obtained by

Wang et a/. (1980). A form ofcytochrome P-450 present in the B2 fraction ofBeaune

et a/. (1980) preparation can be assumed to be unstable, since the cytochrome P-450

preparation by Wang et al. (1980) and the present two cytochrome P-450

preparations, from autopsy sampies, did not show such high activities, in the

82 R. KATO& T. KAMATAKI

oxidation ofethoxycoumarin and benzo[a]pyrene, as did the B2 fraction.

Al n 166.OOll

CDtolase (58.00l)

In 116. t- -

ISTD I • 16 9) c, 6 I

Figure 1 SDS-polyacrylamide gel electrophoresis of partially purified preparations of

cytochromeP-450 from human livermicrosomes. STD, protein standards indicated in the figure wereapplied. Lactatedehydrogenase is shownas

lactate dh.

Trp-P-l, [3-amino-l,4-dimethyl-5-H-pyrido(4,3-b)indole] and Trp-P-2, [3-aminoI-methyl-5-H-pyrido-(4,3-b)indole] are present in charred parts of foods containing

protein and in smoke as the result oftryptophan pyrolysis. Trp-P-I and Trp-P-2, as

weil as benzo(a)pyrene, show potent mutagenic activity after undergoing metabolie

activation by cytochrome P-450 of experimental animals (Ishii , Ando, Kamataki &

Kato, 1980; Yamazoe, Ishii, Kamataki, Kato & Sugimura, 1980). The present work

showed that in contrast to rat liver microsomes, 7,8-benzoflavone stimulated

metabolie activation of Trp-P-2 in human liver microsomes. To confirm the ability

of human cytochrome P-450 to activate Trp-P-I and Trp-P-2, cytochrome P-450

was fractionated into four fractions. Human microsomes, from normal portions ofa

Iiver isolated by operation for hepatic cancer, were treated with cholic acid, and

cytochrome P-450 was fractionated by means of to-amino-n-octyl Sepharose 4B,

Table 1 Comparison ofthe activitiesof cytochrome P-450 purified from human and rat liver

microsomes. Activitiesexpressed, for human liver, as nmol substrate nmol P-450-1 mirr" and,

forrat liver,as nmol substratenmol P-450-1or P-448-1mirr" .

Substrate

Aniline

Aminopyrine

Benzphetamine

7-Methoxycoumarin

7-Ethoxycoumarin

7-Propoxycoumarin

Human

P-450(1) P-450(II)

2.45 0.22

"3 .30 ND···

5.40 0.80

0.18 ND

0.09 0.00

0.04 ND

Rat

PBP-450· MCP-448··

1.90 0.91

14.90 9.70

32.70 7.10

0.79 0.62

4.22 53.20

2.24 45.42

• CytochromeP-450 purifiedfrom phenobarbitone-treatedrats.

•• CytochromeP-448 purifiedfrom3-methylcholanthrene-treated rats. ••• Not determined.

PURIFICATIO N OF HEPA TIC CYTOCHROME P-450 83

hydroxylapatite and CM-Sephadex(C-50) columns. Fractions land 11 were

separated by the hydroxylapatite column and subfractions, I-a , I-b, II-a and II-b ,

were separated by CM -Sephadex columns. As can be seen in Table 2, Fraction I-b

showed relatively high mutagen-producing activity.

Table 2 Metabolie activation oftryptophan pyrolysis products by cytochrome P-450 purified

from human liver microsomes.

Fractions

l-a I-b H-a

(TA 98 revertants plate" , 0.2 nmol P-450)

15* 191 44

75 635 70

Trp-P-I

Trp-P-2

Specific content ofP-450

(nmol mg proteinrl) 5.3 1.2 16.3

H-b

44

129

7.9

* Subtracted by the number ofcontrol revertants, 27.

Pharmacological implications of multiple forms of cytochrome P-450

There are marked differences in the activities of drug metabolizing enzymes between

species and strains of experimental an imals. If human microsomes metabolize a

particular drug, with a similar rate to microsomes from an experimental animal, it

does not necessarily mean that the m icrosomes from man and the experimental

animal contain the same forms ofcytochrome P-450 and at the same level. Thus, the

nature of human drug metabolizing enzymes can not be estimated without using

human sampIes. In addition, racial differences, probably due to genetic and

nutritional differences, have also been noted. Thus, these differences can, at least in

part, be accounted for by the amount and characteristics of one or more forms of

cytochrome P-450 present. Furthermore, it has been established that drug metabolizing activities are changed by pathological and nonphysiological states, in experimental animals (Kato, 1977). The same may be true in man, since pharmacokinetic

studies have indicated significant changes in drug metabolizing activities caused by

endogenous and exogenous factors, such as, disease states and drug inta ke. Thus, the

next challenge must be to determine relative changes in the amounts of multiple

forms of cytochrome P-450 by these numerous factors, and implication of the

presence of multiple forms ofcytochrome P-450 to human therapy. For these experiments, it would be meaningless to analyze data from autopsy sampIes, since most of

the cytochrome P-450 forms might have been degraded. On the other hand, it is

impossible to obtain large amounts of human liver sampies to determine the forms of

cytochrome P-450. With progress in the purification procedure, it will be possible to

extract minor forms of cytochrome P-450 remaining in the autopsy sampIes, if the

sampIes can be treated within one hour after death. Thus, the practical approach may

Table 3 Purposes and benefltsin the puriflcation of cytochrome P-450 from human liver.

I Determination of multiplicity of cytochrome P-450 and preparation ofthe antibody.

2 Quantification ofvarious formsof cytochrome P-450 from small sizeof'biopsy sampies using

the antibody.

3 Resolution ofsome important problems.

i Alterations ofcytochrome P-450 under pathological and nonphysiologicalstates.

ii EtTects ofdrugs, diets and environmental chemicals.

iii Quantitative speciesditTerences in cytochrome P-450.

iv Qualitative and quantitative determinations of genetic ditTerences. v Evaluation ofracial ditTerences through international cooperation in the exchangeofthe

antibodies.

84 R. KA TO & T. KAMATAKI

be to use an antibody method whereby even small amounts of human liver may be

used for the determination of the cytochromes. As mentioned above, there are

marked racial differences in drug metabolism. It is hoped that it will be possible to

exchange antibodies internationally for studies on racial differences of cytochrome

P-450 (Table 3).

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